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3-Chloro-5-trifluoromethylpyridine-2-carboxylic acid, a Metabolite of the Fungicide Fluopyram, Causes Growth Disorder in Vitis viniferaClick to copy article linkArticle link copied!
- Peter RobatscherPeter RobatscherLaimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Peter Robatscher
- Daniela EisensteckenDaniela EisensteckenLaimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Daniela Eisenstecken
- Gerd InnerebnerGerd InnerebnerLaimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Gerd Innerebner
- Christian RoschattChristian RoschattLaimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Christian Roschatt
- Barbara RaiferBarbara RaiferLaimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Barbara Raifer
- Hannes RohreggerHannes RohreggerSouth Tyrolean Extension Service for Fruit- and Winegrowing, Via Andreas Hofer 9/1, IT-39011 Lana, South Tyrol, ItalyMore by Hannes Rohregger
- Hansjörg HafnerHansjörg HafnerSouth Tyrolean Extension Service for Fruit- and Winegrowing, Via Andreas Hofer 9/1, IT-39011 Lana, South Tyrol, ItalyMore by Hansjörg Hafner
- Michael Oberhuber*Michael Oberhuber*Telephone: +39-0471-969510. Fax: +39-0471-969599. E-mail: [email protected]Laimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, ItalyMore by Michael Oberhuber
Abstract
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The aim of this study was to investigate the effect of 3-chloro-5-trifluoromethylpyridine-2-carboxylic acid (PCA), a metabolite of the fungicide fluopyram, on grapevine. During spring and summer 2015, grapevine growth disorders were observed in several countries in Europe. An unprecedented herbicide-like damage was diagnosed on leaves and flowers, causing significant loss of harvest. This study proposes PCA as the causing agent of the observed growth disorders. PCA was shown to cause leaf epinasty, impaired berry development that leads to crop loss, and root growth anomalies in Vitis vinifera similar to auxin herbicides in a dose-dependent manner. Using both field trials and greenhouse experiments, the present study provides first evidence for a link between the application of fluopyram in vineyards 2014, the formation of PCA, and the emergence of growth anomalies in 2015. Our data could be useful to optimize dosage, application time point, and other conditions for an application of fluopyram without phytotoxic effects.
Copyright © 2019 American Chemical Society
Introduction
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Grapevine (Vitis vinifera subsp. vinifera) is one of the world’s most important and most valuable crops, used for table grapes, raisin grapes, and wine production, with an annual wine production of 266 million hL in 2016. (1)V. vinifera vine growers have to develop strategies to protect the crop against pests and diseases. Nowadays, V. vinifera is mostly affected by fungal diseases, including downy mildew (caused by Plasmopara viticola), (2) powdery mildew (caused by Erysiphe necator), (3) and botrytis bunch rot (caused by Botrytis cinerea). (4)
Crop protection strategies in integrated production rely vastly on the use of synthetic fungicides, such as fluopyram, dithianon, folpet, dimethomorph, cyazofamid, zoxamid, spiroxamin, and others. Most synthetic fungicides are target-specific, inhibiting a vital pathway in the disease; however, unwanted side effects can occur by off-target binding of the active ingredient or one of its metabolites. (5) Fungicides like copper can inhibit photosynthesis; benzimidazoles, anilides, and pyrimidines can have phytotoxic effects on plants; (6) and difenoconazole can cause injuries in some cold-climate wine grapes after (repeated) applications. (7) Yield losses and smaller fruit size are reported side effects of sulfur-based fungicides in organic pipfruit production. (8)
Fluopyram belongs to the chemical class of N-(pyridylethyl)benzamides and has been approved in the European Union (EU) since 2013 as a fungicide to control powdery mildew, botrytis bunch rot, apple scab, and other fungal diseases. Fluopyram is metabolized in plants by hydroxylation at C-7 or C-8, (9) followed by cleavage or glycosylation. A total of five metabolites were identified in V. vinifera using 14C-labeled fluopyram, including 2-(trifluoromethyl)benzamide and 3-chloro-5-trifluoromethylpyridine-2-carboxylic acid (PCA; Figure 1). Fluopyram acts as succinate dehydrogenase inhibitor (SDHI) and was widely used as botryticide in European wine growing regions during 2014. In South Tyrol, Italy, the 2014 season was extraordinarily rainy, with precipitation exceeding the 10 year average by over 30% in Bolzano/Bozen. (10) As a consequence, fluopyram was widely used in South Tyrol to control B. cinera with repeated applications in summer (end of July) using a dosage of 250 g of active ingredient (ai)/ha each. In 2015, between May and June, unprecedented symptoms of anomalous growth and berry development (Figure 2) were observed in vineyards throughout Europe, including Italy, Germany, Switzerland, France, and Luxemburg. Leaves developed a jellyfish-type shape, resembling symptoms of auxin-inhibiting herbicides, and berry development was impaired because flowerhoods did not detach from the receptacle, leading to significant losses in the 2015 vintage. The phenomenon was reported from several countries, (11) but its causes remained enigmatic. Meteorological conditions, including the extraordinarily high precipitation in the region during the 2014 season (132.7 mm in July 2014 at Bozen/Bolzano compared to 29.3 and 85.9 mm in July 2013 and July 2012, respectively), (10) gave first hints but were not sufficient to explain the observations alone. When plant protection measures were compared to previous years, treatment with fluopyram (in the form of the commercial product Luna Privilege) emerged as a significant difference in the season preceding the symptoms. The fungicide was introduced in Italy in 2012 and tested in Laimburg Research Centre’s experimental fields during 2012–2014 as well as for registration purposes in other 17 different vineyards located in North and South Europe; (9) however, growth anomalies have not been reported. The product was broadly used in South Tyrol for the first time during the 2014 season. A total of 3096.57 ha (56.9% of the total area under vine) was treated to control B. cinera; in addition, the meteorological conditions in 2014 required a repeated application, resulting in a widespread and high-dose exposure of grapevines to fluopyram. These findings provided the basis to hypothesize a link between the growth anomalies and the fluopyram treatments. The link was further supported by the striking structural similarity of one metabolite [3-chloro-5-trifluoromethylpyridine-2-carboxylic acid (PCA)], with auxin herbicides of the pyridine carboxylic acid group like clopyralid (Figure 1).
Figure 1
Figure 1. Constitutional formulas of fluopyram and fluopicolide and metabolites of fluopyram in V. vinifera leaves (left) and formula of the herbicide clopyralid (bottom right). Fluopyram-8-OH, N-{2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-1-hydroxyethyl}-2-(trifluoromethyl)benzamide; fluopyram-7-OH, N-{2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-2-hydroxyethyl}-2-(trifluoromethyl)benzamide; and fluopyram-7-OGlc, N-[2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-2-(β-glucopyranosyloxy)ethyl]-2-(trifluoromethyl)benzamide (fluopyram numbering according to ref (9)).
Figure 2
Figure 2. Growth distortion symptoms on V. vinifera flowers and leaves. (Left) Leaf symptom index (SI; 0, asymptomatic/no distortion (not shown); 1, light; 2, intermediate; and 3, strong distortion on leaves) and grape symptom index (SI; 0, no loss of berries in grape clusters (not shown); 1, 1–33% loss; 2, 33–66% loss; and 3, 66–100% loss), (center) symptomatic leaves from fluopyram-treated commercial vineyards (i) and symptoms on new grown leaves after PCA treatment (ii), and (right) symptomatic grapes from fluopyram-treated commercial vineyards (iii). Pictures of grapes SI 1 and 2 are at phenology stage BBCH = 73, and grapes SI 3 and affected grapes from commercial fields (iii) are at phenology stage BBCH = 71–73.
This work reports on an investigation on the causes of the observed growth anomalies, focusing on possible undesired effects of the fungicide fluopyram and its metabolites. The study provides, to the best of our knowledge, the first evidence linking a fluopyram metabolite to growth disorders with concomitant economic losses.
Material and Methods
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Reagents
PCA for experimental trials was obtained from Georganics, Ltd. (Bratislava, Slovakia); 2-trifluoromethylbenzamide and 2-(trifluoromethyl)benzoic acid were obtained from Sigma-Aldrich (Milan, Italy); [3-chloro-5-(trifluoromethyl)pyridin-2-yl]acetic acid was obtained from AKOS Consulting & Solution GmbH (Steinen, Germany). Luna Privilege (41.66% fluopyram), Century SL (51.7% potassium phosphonate), and R6 Erresei Albis (4.44% fluopicolide and 66.67% fosetyl-aluminum) were obtained from Landwirtschaftliche Hauptgenossenschaft Südtirol (Bolzano, Italy). Analytical standards (PCA and fluopyram), acetonitrile [liquid chromatography–mass spectrometry (LC–MS) grade], formic acid (LC–MS grade) were obtained from Sigma-Aldrich. Water was deionized using a Milli-Q Integral 15 system from Merck Millipore (Milan, Italy).
Survey of Symptoms in Commercial Fields
During the 2015 vintage, data on crop loss in all vineyards in South Tyrol, Italy, in which growth anomalies had been reported during the spring of that year, were collected (Table 1). Vineyards were classified by visual inspection in four groups depending upon the degree of crop loss (0–25, 25–50, 50–75, and 75–100%).
Table 1. Vineyards Affected by Fluopyram-Related Crop Loss (Expressed as a Percentage of Averaged Crop Loss Compared to the Three Previous Seasons in the Same Vineyard) during 2015 (Columns 2–6) and Total Cultivation Area Per V. vinifera Cultivar (Column 7)
| cultivation area (ha) with crop loss 2015 (fluopyram treatment 2014) | ||||||
|---|---|---|---|---|---|---|
| V. vinifera cultivar | 0–25% | 25–50% | 50–75% | 75–100% | total (ha) | cultivation area in South Tyrol (ha) |
| Sauvignon blanc | 38.48 | 65.83 | 21.47 | 6.01 | 131.79 | 381 |
| Chardonnay | 35.88 | 19.38 | 7.59 | 1.87 | 64.72 | 529 |
| Gewürztraminer | 27.14 | 20.25 | 3.26 | 0.00 | 50.65 | 572 |
| Pinot blanc | 21.42 | 11.52 | 2.97 | 0.20 | 36.11 | 521 |
| Cabernet sauvignon | 7.86 | 7.89 | 1.96 | 1.75 | 19.46 | 158 |
| Pinot gris | 8.12 | 4.21 | 1.56 | 0.00 | 13.89 | 627 |
| Pinot noir | 11.19 | 0.64 | 0.74 | 0.59 | 13.16 | 417 |
| Yellow Muscat | 6.34 | 5.06 | 1.75 | 0.00 | 13.15 | 88 |
| Müller Thurgau | 9.00 | 3.39 | 0.47 | 0.00 | 12.86 | 221 |
| Lagrein | 4.60 | 2.88 | 1.83 | 0.19 | 9.5 | 452 |
| Vernatsch | 6.68 | 1.64 | 0.15 | 0.30 | 8.77 | 849 |
| Silvaner | 6.21 | 0.71 | 1.01 | 0.00 | 7.93 | 71 |
| Merlot | 3.15 | 2.22 | 1.29 | 0.22 | 6.88 | 186 |
| Kerner | 2.87 | 2.16 | 0.00 | 0.29 | 5.32 | 92 |
| Riesling | 3.74 | 0.53 | 0.00 | 0.00 | 4.27 | 67 |
| Moscato rosa | 0.45 | 0.35 | 0.00 | 0.33 | 1.13 | 15 |
| Veltliner | 0.54 | 0.00 | 0.00 | 0.00 | 0.54 | 27 |
| various | 0.00 | 0.00 | 0.38 | 0.00 | 0.38 | 93 |
| Zweigelt | 0.00 | 0.34 | 0.00 | 0.00 | 0.34 | 30 |
| total (ha) | 193.67 | 149.00 | 46.43 | 11.75 | 400.85 | 5396.00 |
| area treated with fluopyram (ha) | 3039.57 | |||||
Symptom Indices (SIs) on Leaves and Grapes
SIs were defined for leaves depending upon the severity of the anomalies and for grapes depending upon the proportion of undeveloped berries, with 0 indicating no anomalies, 1 indicating light distortions (leaf, spiny margins on ca. 50% of the new grown apical leaves; grape, 0–33%), 2 indicating intermediate distortions (leaf, irregular dentate margins on ca. 50% of the new grown apical leaves; grape, 33–66%), and 3 indicating severe distortions (leaf, irregular dentate margins, with a jellyfish shape on ca. 75% of the new grown apical leaves; grape, 66–100%; see Figure 2).
Field Trials
V. vinifera cv. Gewürztraminer (planted in 1997, single Guyot training system) cultivated in an experimental field at 240 m above sea level (asl) (“Stadlhof” vineyard, Laimburg, Italy; GPS coordinates, 46° 22′ 57.5″ N, 11° 17′ 02.1″ E; soil type, slightly loamy sand), cv. Chardonnay (planted in 1999, single Guyot training system, “Hausanger” vineyard, Laimburg, Italy; at 230 m asl; GPS coordinates, 46° 22′ 52.5″ N, 11° 17′ 09.5″ E; soil type, silty sand), and cv. Sauvignon blanc (planted in 2006, single Guyot training system, “Piglon” vineyard, Laimburg, Italy; 240 m asl; GPS of the vineyard, 46° 21′ 35.2″ N, 11° 17′ 06.8″ E; soil type, sandy clay) were used for this study. The plants were grown according to the regional guidelines for integrated pest management involving treatments with indoxacarb, cyazofamide (2 times), metrafenone, zoxamide (2 times), copper hydroxide (4 times), cyflufenamide (2 times), sulfur (4 times), tetraconazole (2 times), and spiroxamine (2 times). Chardonnay and Gewürztraminer were treated additionally with bupirimate and boron foliar fertilizer (2 times); Chardonnay was treated additionally with gibberellic acid; and Sauvignon was treated additionally with fluopicolide, mineral oil, and boron–calcium foliar fertilizer. Three herbicide applications with glyphosate (1080 g ha–1) were carried out, but no auxin herbicides were used in the years preceding the experiment.
Preliminary field experiments: “PCA-spray on foliage”: Two plants (Gewürztraminer, “Stadlhof” vineyard) at phenology stage Biologische Bundesanstalt, Bundessortenamt and Chemische Industrie (BBCH) = 73–75 were treated with 0.1% aqueous PCA (w/v, 250 mL per plant by foliar application with a spray lance) on July 9, 2015. Two neighboring plants were left untreated as the control. Five symptomatic leaves were collected from each plant on Aug 18, 2015 and Sept 4, 2015. This experiment was repeated in the same field with a treatment on Aug 28, 2015 and monitored for symptoms until June 9, 2016. “PCA-injection”: Two plants (Gewürztraminer, “Stadlhof” vineyard) at phenology stage BBCH = 75–77 were treated with PCA by injecting 0.1% aqueous PCA (w/v, 100 μL per plant) into the internode 7 on July 23, 2015. A total of 100 μL of water was injected into one neighboring plant as the control. Five symptomatic leaves from each plant were collected on Sept 3, 2015 or Sept 4, 2015.
“High dose foliar fluopyram treatment on three cultivars”: Gewürztraminer Chardonnay, and Sauvignon blanc from the “Stadlhof”, “Hausanger”, and “Piglon” experimental fields, respectively, were treated with a 3-fold dose of fluopyram (250 g of ai ha–1 recommended and 750 g of ai ha–1 applied) using a spray lance. For each cultivar, four different treatments were applied: treatment 1 involved the commercial product (Luna Privilege, obtained in 2014), treatment 2 involved the commercial product obtained in 2015, treatment 3 involved the commercial product obtained in 2014 with potassium phosphonate (0.302%, using Century SL), treatment 4 involved the commercial product obtained in 2014 with fluopicolide (0.013%) and fosetyl-aluminum (0.2%, using R6 Erresei Albis). For each treatment, three blocks of 12 neighboring plants in separate Guyot rows (in total 36 plants) were sprayed on July 1, 2015 (BBCH = 73–75) and July 30, 2015 (BBCH = 77) with a spray lance. Another three blocks of 12 neighboring plants per variety was left untreated as the control. Leaf and grape symptoms were monitored throughout the season and the year after the treatment (leaf symptoms at BBCH = 53−57, 79, and 89; grape symptoms at BBCH = 79 and 89). Leaf samples of 10 symptomatic leaves were randomly collected from each treatment group the year after application at BBCH = 53−57.
Greenhouse Trials with PCA and Other Fluopyram Metabolites Using Potted Plants
V. vinifera plants Sauvignon blanc and Gewürztraminer (virus-free certified plants: Sauvignon blanc clone 36 Lb grafted on rootstock Fercal 242 and Gewürztraminer clone 48 fr grafted on R110 ISV1 potted on July 22, 2015 and Aug 05, 2015, respectively) were obtained from Battisti Rebschule–Vivai (Caldaro/Kaltern, Italy) and grown in 4.5 L containers (15 × 15 × 40 cm) under greenhouse conditions (temperature, 20–30 °C; sunlight, 7–9 h/day; and relative humidity, 70–90%). All plants were irrigated manually as needed. The dose–response relationship was analyzed by foliar treatment of three plants per cultivar with aqueous PCA (0.0032, 0.008, 0.02, and 0.1%, w/v, 220 mL per plant) on Aug 28, 2015. Three additional plants (one Sauvignon blanc and two Gewürztraminer) were left untreated and used as the control. Leaf symptoms were monitored for a period of 63 days. A second dose–response experiment was performed on Gewürztraminer involving soil application of 5 mL of 0.1% (w/v) aqueous PCA on two plants (corresponding to 5 mg per plant, treated on Aug 27, 2015) and 50 mL of 0.1% (w/v) aqueous PCA on other two plants (corresponding to 50 mg per plant, treated on Aug 27, 2015). Two untreated plants were used as the control, and leaf symptoms were monitored. The effect of PCA on root growth was evaluated on Gewürztraminer by visual inspection of the whole-vine roots 69 and 70 days after treatments using selected samples of the dose–response relationship experiments, including the 0.1 and 0.02% PCA foliar and soil-treated plants and controls. At 80 days after soil application, samples consisting of three symptomatic leaves and three asymptomatic leaves from each treated plant were collected, except for the 50 mL soil application, where only one plant was sampled.
Other metabolites of fluopyram were tested on three potted Sauvignon blanc plants each by foliar spray treatment on Aug 28, 2015 using 0.08% aqueous 2-(trifluoromethyl)benzamide, 0.08% aqueous 2-(trifluoromethyl)benzoic acid, and 0.11% aqueous [3-chloro-5-(trifluoromethyl)pyridin-2-yl]acetic acid).
Leaf Samples from Commercial Vineyards
V. vinifera leaf samples from 10 commercial vineyards (Unterland-Überetsch area, South Tyrol, Italy), which had been treated during 2014 with a commercial product as well as a control sample from an organic vineyard in the region were collected on June 22, 2015 (BBCH = 71–73). Each sample consisted of 10 symptomatic leaves per vineyard collected from 10 grapevines distributed over the vineyard and pooled for PCA analysis. The vines were chosen to be representative for the SI that was assigned to the vineyard.
Analysis of PCA and Fluopyram in Collected Leaf Samples
Leaf samples were immediately transported to the laboratory, frozen at −80 °C for 2 h, crushed manually into small pieces of 2–3 mm, and stored at −28 °C until further analysis. For leaf samples with a higher concentration of PCA (≥0.25 mg kg–1), 5 g of crushed material was extracted with acetonitrile/water/formic acid (80:19.5:0.5, v/v/v, 20 mL) at room temperature (RT) for 1 h. The resulting slurry was centrifuged (5 min at 4000 rpm and RT), and the supernatant was filtered [polytetrafluoroethylene (PTFE), 0.20 μm] and used for LC–MS analysis. To detect traces of PCA and fluopyram (<0.25 mg kg–1), 10 g of leaf material was extracted 2 times with acetonitrile/water/formic acid (85:14.5:0.5, v/v/v, 10 mL) at RT for 1 h each. The combined slurries were centrifuged and filtered as described above, concentrated to dryness under reduced pressure on a rotary evaporator system (Rotavapor R-210, Büchi, Switzerland), and reconstituted in acetonitrile/water/formic acid (85:14.5:0.5, v/v/v, 2.0 mL). The resulting extract was analyzed in single runs by high-performance liquid chromatography (HPLC, Dionex Ultimate 3000, Thermo Fisher, Waltham, MA, U.S.A.; column, Poroshell 120 EC-C18, 3 × 150 mm, 2.7 μm, Agilent, Santa Clara, CA, U.S.A.; precolumn, Poroshell 120 UHPLC Guard EC-C18, 3 mm; and column temperature, 40 °C) using a water/acetonitrile gradient with 0.1% formic acid (solvent A, 0.1% formic acid in water; solvent B, 0.1% formic acid in acetonitrile; and gradient, 0 min, 90% A; 20 min, 63.3% A; 24 min, 5% A; 29 min, 5% A; 33 min, 90% A; and 40 min, 90% A). Analytes were detected using a high-resolution time-of-flight mass spectrometer (HR-TOF–MS, IMPACT HD, Bruker, Billerica, MA, U.S.A.) using negative (PCA) or positive (fluopyram) electrospray ionization. Compounds were identified using the retention time and accurate mass of the quasi-molecular ion peak (PCA, m/z 223.9726; fluopyram, m/z 397.0542) and a fragment ion (PCA, m/z 179.9827) and quantified using an external calibration with commercial PCA and fluopyram standards.
Results
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Harvest losses were recorded during the 2015 vintage for all vineyards in South Tyrol, Italy, in which growth anomalies had been reported during the spring of that year (Table 1). Crop loss was observed on 400.85 ha (13.2% of the total area under vine of 5396 ha): 11.75 ha was affected by severe losses of 75–100%, and 46.43, 149.00, and 193.67 ha were affected by losses of 50–75, 25–50, and 0–25%, respectively. Notably, some cultivars had a higher incidence of symptoms than others. Sauvignon blanc, for instance, was the most affected cultivar, with crop loss being observed on 131.79 ha or 34.5% of its area under vine. Other cultivars with significant losses were Chardonnay and Gewürztraminer, whereas red grapes, including the frequently cropped Vernatsch and Lagrein cultivars, showed minimal losses (Table 1).
To test the hypothesized link between fluopyram, its metabolite PCA, and the emergence of growth anomalies, a 0.1% aqueous solution of PCA was sprayed on Gewürztraminer foliage during early summer 2015 (July 09, 2015; BBCH = 73–75) in an experimental vineyard (“Stadlhof” vineyard). At 10–14 days after application, symptoms were observed on newly grown leaves (Figure 2 and Table 2); the already developed leaves on treated plants, instead, were not affected. Symptomatic leaves were found to contain 0.71 ± 0.53 mg kg–1 of PCA. Untreated control plants did not develop symptomatic leaves. When PCA was applied by injection into the internodes or through the soil, similar symptoms were observed on newly grown leaves, albeit uptake and development of symptoms took longer in the soil application. Injection of water and untreated control plants did not develop anomalous leaves (Table 2). Notably, Gewürztraminer vines in the “Stadlhof” vineyard treated in late summer (Aug 28, 2015; BBCH = 85–89) remained asymptomatic in 2015 but developed leaf and grape SI = 3 in 2016 (Table 2).
Table 2. Concentration of PCA Found in Regrown Symptomatic Leaves after PCA Treatments Involving Different Application Methods (Lines 1–4 Applied on Trial Field Plants and Lines 5–7 Applied on Potted Plants)
| application | treatment with | leaf symptoms observed after | PCA in symptomatic leaves (mg kg–1 of FW ± standard deviation) |
|---|---|---|---|
| spray on foliage | 0.1% PCA (220 mL) | 10–14 daysa | 0.71 ± 0.53 (n = 2) |
| control (untreated) | not observed | ||
| injection | 1% PCA (0.1 mL) | 10–14 days | 0.55 ± 0.19 (n = 2) |
| control (0.1 mL of water) | not observed | ||
| soil | 0.1% PCA (5 mL) | 20–28 days | 0.21 ± 0.03 (n = 2)b |
| 0.1% PCA (50 mL) | 7–20 days | 1.84 (n = 1)b | |
| control (untreated) | not observed |
a
Treatment was on July 09, 2015. When the experiment was repeated on Aug 28, 2015, no symptoms emerged in 2015 but severe symptoms (leaf and grape SI = 3) developed in 2016.
b
Asymptomatic leaves contained 0.04 ± 0.01 mg kg–1 (5 mL dose; n = 2) and 1.0 ± 0.6 mg kg–1 (50 mL dose; n = 2).
Next, the dose dependence was analyzed using potted plants under controlled greenhouse conditions. Potted plants (Sauvignon blanc and Gewürztraminer) were treated with aqueous 0.1, 0.02, 0.008, and 0.0032% PCA, respectively. Similar to the results in the experimental field, vines (Sauvignon blanc) treated with 0.1% PCA developed leaves with SI = 3 after less than 1 week. PCA at 0.02% lead to plants with leaf SI = 2 after 19 days and SI = 3 after 27 days. Vines treated with 0.008 and 0.0032% PCA remained asymptomatic for a longer period but ultimately, after 56 days, developed symptomatic leaves with SI = 2 and 1, respectively (Figure 3). The experiment was repeated with Gewürztraminer, confirming the dose–response relationship and the observation that Gewürztraminer developed less severe symptoms than Sauvignon blanc (Figure 3). None of the vines recovered to a lower SI, and none of the leaves recovered to asymptomatic once the first growth anomalies had been detected. The untreated control plants, however, were asymptomatic throughout the experiment (Figure 3). A similar dose-dependent development of symptomatic leaves was observed when PCA was applied through the soil in two doses (5 and 50 mL of 0.1% PCA, respectively; Table 2). Untreated control plants remained asymptomatic. After 69 days, the soil was removed from the potted vines, revealing a growth depression of the roots by visual inspection. Vines treated with 0.02% PCA showed a marked inhibition of root growth compared to roots from control plants (Figure 4). Even though the number of treated plants was low, a dose-dependent inhibition of root growth after foliar PCA treatment was noted. The concentration of PCA in symptomatic leaves correlated with the amount of PCA applied in the soil (Table 2), but traces of PCA were also detected in asymptomatic leaves (0.04 mg kg–1 of PCA content in leaves for 5 mg of PCA soil application per plant and 1.0 mg kg–1 of PCA for the 50 mg application of PCA per plant).
Figure 3
Figure 4
Figure 4. Root development of potted vines cv. Gewürztraminer after foliar treatment with 0.02% PCA (left) and control plants (right).
To test whether the same symptoms could be triggered by the application of fluopyram and consequent decay to PCA, three grapevine cultivars (Sauvignon blanc, Chardonnay, and Gewürztraminer in the “Piglon”, “Hausanger”, and “Stadlhof” vineyards, respectively) were treated with a 3-fold overdose of fluopyram in a field trial on July 1, 2015 and July 30, 2015. In addition, each cultivar was treated with the commercial product of two different production years (treatments 1 and 2 in Table 3) and in combination with other plant protection products (treatments 3 and 4 in Table 3), which were typically sprayed together with fluopyram in commercial vineyards during 2014. Fluopicolide was added to test the effect of a second PCA source. (12) After this treatment in 2015, the plants were monitored throughout the season and the following year: first weak symptoms on leaves of Sauvignon blanc were observed in fall 2015 (SI = 1) and confirmed in 2016, when the vines developed a leaf SI = 1–2 at inflorescence (BBCH = 53–57) and remained symptomatic for the whole season (Table 3). Also, berry development was seriously impaired in a way similar to the affected commercial vineyards (grape SI = 2–3 from touching until ripening; BBCH = 79 to 85–89). The symptoms on Sauvignon blanc were one SI class lower at BBCH = 53–57 and 79 when treated with the 2015 formulation (treatment 2 in Table 3) and one SI class higher for the treatments 3 and 4 at BBCH = 85–89, but in general, neither the production year nor the addition of other plant protection products, including fluopicolide, had a significant impact on the symptom development (Table 3). Importantly, untreated control plants did not show symptoms on leaves or grapes. Leaves from treated plants contained residues of fluopyram (0.09–0.25 mg kg–1 on Sauvignon blanc; Table 3) and PCA (0.01–0.02 mg kg–1), even though the fungicide had been sprayed 1 year before and the whole foliage as well as most of the 1-year-old wood had been removed by dormant pruning. Despite this significant removal of contaminated plant material, symptomatic leaves and flowers were observed on shoots emerging from dormant buds in the following year, confirming the hypothesis that fluopyram treatment can cause growth anomalies several months after its application. Gewürztraminer and Chardonnay showed similar results but on average developed less severe symptoms on both grapes (SI = 1–3 and 1–2, respectively) and leaves (SI = 1–2) and had lower residues of fluopyram. PCA was at or below the limit of quantification (Table 3).
Table 3. Effect of Treatment with an Overdose (3-Fold Recommended) of Fluopyram (Luna Privilege, Alone and in Combination with Other Plant Protection Products) on Three Grapevine Cultivars (Treatment Dates of July 1, 2015 and July 30, 2015)a
| leaf SI, year 2016 | grape SI, year 2016 | PCA in symptomatic leaves (mg kg–1 of FW) | fluopyram in symptomatic leaves (mg kg–1 of FW) | ||||
|---|---|---|---|---|---|---|---|
| V. vinifera cultivar | inflorescence, BBCH = 53–57 | berries touching, BBCH = 79 | ripening, BBCH = 85–89 | berries touching, BBCH = 79 | ripening, BBCH = 85–89 | inflorescence, BBCH = 53–57 | inflorescence, BBCH = 53–57 |
| Sauvignon blanc | |||||||
| treatment 1 | 2 | 1 | 1 | 3 | 2 | 0.01 | 0.19 |
| treatment 2 | 1 | 1 | 1 | 2 | 2 | 0.01 | 0.09 |
| treatment 3 | 2 | 1 | 1 | 3 | 3 | 0.01 | 0.15 |
| treatment 4 | 2 | 1 | 1 | 3 | 3 | 0.02 | 0.25 |
| control (untreated) | 0 | 0 | 0 | 0 | 0 | ||
| Gewürztraminer | |||||||
| treatment 1 | 1 | 1 | 1 | 1 | 2 | nd | 0.11 |
| treatment 2 | 1 | 1 | 1 | 2 | 2 | 0.01 | 0.07 |
| treatment 3 | 2 | 2 | 1 | 2 | 2 | 0.01 | 0.02 |
| treatment 4 | 2 | 2 | 1 | 3 | 2 | 0.01 | 0.03 |
| control (untreated) | 0 | 0 | 0 | 0 | 0 | ||
| Chardonnay | |||||||
| treatment 1 | 1 | 1 | 1 | 1 | 1 | nd | 0.04 |
| treatment 2 | 1 | 1 | 1 | 1 | 1 | nd | 0.02 |
| treatment 3 | 1 | 1 | 1 | 2 | 1 | 0.01 | 0.03 |
| treatment 4 | 2 | 1 | 1 | 2 | 1 | 0.01 | 0.02 |
| control (untreated) | 0 | 0 | 0 | 0 | 0 | ||
a
Treatment 1, commercial product of fluopyram 2014; treatment 2, commercial product of fluopyram 2015; treatment 3, commercial product of fluopyram 2014 with potassium phosphonate (0.302%); and treatment 4, commercial product of fluopyram 2014 with fluopicolide (0.013%) and fosetyl-aluminium (0.2%). Symptoms, PCA and fluopyram contents in the year following the application. SI: 1, light symptoms; 2, intermediate symptoms; 3, strong symptoms on leaves and grapes, respectively (see Figure 2). FW, fresh weight; nd, not detected.
To validate the preliminary results from the field trial in commercial vineyards, the data collected in South Tyrolean vineyards during the 2015 season (Table 1) and the corresponding crop protection registers of the previous year were analyzed. In addition, leaf samples collected in 2015 were analyzed for residues of fluopyram and PCA. All leaves except for one untreated organic vineyard (entry 11 in Table 4) contained fluopyram in the range between 0.03 and 0.06 mg kg–1. In addition, all but the organic vineyard and one of the Chardonnay fields (entry 4) were tested positive for PCA. However, the amount of residual fluopyram and PCA did not correlate perfectly with the symptom indices. Vineyard 8, for instance, was not affected by crop loss, but leaves were analyzed with 0.04 mg kg–1 PCA, suggesting that additional variables for the development of symptoms, such as the application time point, the pruning and training system, other agricultural practices, or the site, might play a role. Our data support a relevant role, in particular, for the application time point: vines in the “spray on foliage” experiment treated with PCA in July 2015 developed epinastic leafs within 14 days (Table 2) but showed only light symptoms in spring 2016 (SI = 1), whereas the vines treated in late August 2015 remained asymptomatic during 2015 but developed leaf and grape SI = 3 during the following year (Table 2).
Table 4. Concentration of Fluopyram and PCA in Symptomatic Leaves from Commercial Vineyardsa
| vineyard | V. vinifera cultivar | location | treatment date fluopyram | grape SI | PCA in symptomatic leaves (mg kg–1) | fluopyram in symptomatic leaves (mg kg–1) |
|---|---|---|---|---|---|---|
| 1 | Sauvignon blanc | Andrian | July 10, 2014 | 3 | 0.02 | 0.04 |
| 2 | Sauvignon blanc | St. Pauls | July 28, 2014 | 3 | 0.01 | 0.04 |
| 3 | Chardonnay | St. Pauls | July 23, 2014 | 3 | nd | 0.06 |
| 4 | Sauvignon blanc | Girlan | Aug 4, 2014 | 3 | 0.01 | 0.03 |
| 5 | Chardonnay | Girlan | Aug 4, 2014 | 3 | 0.01 | 0.03 |
| 6 | Sauvignon blanc | Eppan | na | 2 | 0.01 | 0.03 |
| 7 | Chardonnay (Guyot system) | Kaltern | July 25, 2014 | 3 | 0.02 | 0.03 |
| 8 | Chardonnay (Pergel system) | Kaltern | July 25, 2014 | 0 | 0.04 | 0.03 |
| 9 | Sauvignon blanc | Montan | na | 0 | 0.03 | 0.03 |
| 10 | Sauvignon blanc | Montan | na | na | 0.02 | 0.05 |
| 11 | Sauvignon blanc, organic | Andrian | not treated | 0 | nd | nd |
a
All samples were collected on June 22, 2015 from fluopyram-treated vineyards in 2014. nd, not detected; na, not available.
Besides PCA, other metabolites of fluopyram, including 2-(trifluoromethyl)benzamide, 2-(trifluoromethyl)benzoic acid, and [3-chloro-5-(trifluoromethyl)pyridin-2-yl]acetic acid), were considered and tested by spraying on potted plants (Figure 1). None of them shared structural features with a known auxin herbicide. Potted plants were asymptomatic after foliar treatment with 0.08% aqueous 2-(trifluoromethyl)benzamide, 0.08% aqueous 2-(trifluoromethyl)benzoic acid, and 0.11% aqueous [3-chloro-5-(trifluoromethyl)pyridin-2-yl]acetic acid), respectively, confirming that these fluopyram metabolites were not able to give rise to growth anomalies.
Discussion
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Auxin herbicides are synthetic compounds that exploit the function of natural auxin phytohormones, including indole-3-acetic acid (IAA). At a constant high concentration, (13−17) auxin herbicides trigger molecular events, known as auxin overdose, that lead to growth anomalies and, ultimately, to cell death. (18) IAA and synthetic analogues, such as 2-methoxy-3,5-dichloro-benzoic acid (dicamba) and 3,5-dichloro-pyridine-2-carboxylic acid (clopyralide), (19,20) have been shown to bind to a variety of plant receptors, including the auxin binding protein (ABP1) (21−23) and the transport inhibitor response (TIR1) protein, (24−27) which trigger a deregulated growth phase, followed by growth inhibition and cell death. (18) During the growth phase, the transcription of auxin response genes boosts ethylene biosynthesis in the shoots, leading to a downward curvature of leaves (leaf epinasty). (18) Leaf epinasty, thought to derive from asymmetric growth rates of the top and bottom side of the leaf, was the most evident symptom in V. vinifera growth anomalies (Figure 2). Computation models have highlighted the importance of the carboxylic acid function and the ring system for TIR1 binding. (18) PCA shares important structural features with clopyralide and other auxin herbicides: a carboxylic function with a N-heterocycle in the α, β, or γ position and halogen (or a chemically equivalent trifluoromethyl) substituents in the ring system. These structure–activity similarities suggest that the herbicide-like leaf epinasty and flowering anomalies could be symptoms of an auxin overdose-type reaction of the plant to PCA. Other fluopyram metabolites, such as 2-(trifluoromethyl)benzamide, 2-(trifluoromethyl)benzoic acid, and [3-chloro-5-(trifluoromethyl)pyridin-2-yl]acetic acid), lack the pyridine carboxylic acid moiety and were not able to elicit the observed growth anomalies, even though the benzamides share some structural features with the herbicide dicamba. These findings support the auxin overdose hypothesis, but more research is needed to understand the molecular details of PCA action.
Metabolic transformations in V. vinifera have been shown to convert fluopyram into PCA with a relative abundance of ca. 0.8% under typical conditions. (9,28) Our studies confirmed that PCA is detectable in fluopyram-treated plants, which show the same symptoms as PCA-treated plants (Tables 2–4). Fluopyram itself and other metabolites were not able to cause growth anomalies. The concentrations of fluopyram used in our field trials were 3-fold compared to the recommended application doses. Nevertheless, PCA concentrations found in epinastic leaves in commercial vineyards (Table 4) were on the same order of magnitude as those found in our trials (Table 3). Under the controlled conditions in the field trials, PCA concentrations correlated well with the symptom indices (Table 3), suggesting a clear dose–response relationship. However, in the commercial fields, the correlation was less clear. For instance, PCA-containing leaves were found in two vineyards without crop loss in 2015 (Table 4). In addition, in the greenhouse trials, PCA was detected also in asymptomatic newly grown leaves, albeit in lower concentrations (Table 2). Registration data of fluopyram report traces of PCA in leaves (28) as well, but growth anomalies were not known before 2015. Clearly, more research is needed to better elucidate all environmental and molecular triggers of the observed growth anomalies.
One key factor may have been the rainy 2014 season, which required high dosage of fluopyram and/or caused the product to build up in the plant over time. PCA-treated plants in our study were exposed to high concentrations but developed symptoms on regrown leaves immediately after treatment. Our data confirm that the lag phase (time between treatment and emergence of symptoms) and the SI depend upon the PCA dose and time point (Figure 3). In addition, they show that PCA was transported both acropetally and basipetally; this can be rationalized with the zwitterionic structure of PCA, carrying a positive and negative charge under physiological conditions, which is well-known to be transported in both the xylem and phloem system. (14) Therefore, it can be concluded that PCA, formed as a metabolite after fluopyram applications in the field, was accumulating during late summer and fall of 2014/2015 in the plants, in particular in the woody tissue of the vine (cordon, trunk, and perhaps even roots, depending upon the level of transport), and possibly caused an auxin overdose situation, giving rise to growth anomalies, including leaf epinasty. It is important to note that the extraordinarily wet 2014 season (10) required multiple and, in particular, late fluopyram treatments to control Botrytis. The late (Aug 28, 2015) treatment in the “spray on foliage” experiment confirmed this scenario: symptoms were not evident in fall 2015, because new growth is limited; in spring 2016, instead, severe leaf and grape symptoms were observed. The potted plants were also treated in August 2015 and developed symptoms earlier; however, they cannot be compared, because their phenology stage and growth conditions were substantially different. New growth in vineyards is limited in fall, making it plausible that symptoms were not observed in the same year.
Additional factors appear to play a role in symptom development, the most evident of which are the application time point and the different incidences of the analyzed cultivars, as observed in the field trails and the greenhouse experiment. The lower fluopyram and PCA contents in leaves of Gewürztraminer and Chardonnay give some hints to a possible differential uptake, but more research is needed to understand the crucial factors for PCA phytotoxicity, including the application time point, the cultivar, the factors affecting the metabolism of fluopyram, the training system, and others.
High fluopyram concentrations present in vineyards in late summer and fall 2014 are proposed to have been metabolized to accumulate phytotoxic concentrations of PCA in fall and during the dormant season (29) that became evident as leaf epinasty in spring 2015 and crop loss in vineyards in South Tyrol, Italy, and other parts of Europe. These symptoms may not have been observed in previous years and in the registration trials because fluopyram was applied in lower dosage and/or earlier in the season, avoiding phytotoxic concentrations of PCA. It is important to note that, even in 2015, only 13.5% of the treated area in South Tyrol, Italy, was affected by growth anomalies, whereas the rest was asymptomatic. In addition, the growth anomalies differed in incidence and severity, suggesting that there is a regime of safe application of fluopyram.
This study suggests that PCA, a metabolite of the fungicide fluopyram, can cause leaf epinasty and an impaired berry development that leads to crop loss on V. vinifera similar to auxin herbicides. The present work provides first evidence for a link between the application of fluopyram in vineyards, the formation of PCA, and the emergence of growth anomalies in the following year. These data could be useful to optimize dosage, application time point, and other conditions for a safe application of fluopyram without phytotoxic effects; however, our understanding of the exact conditions and molecular pathways leading to the observed anomalies is far from complete. Future research should investigate the metabolism of fluopyram in more detail under different environmental conditions, conclusively determine the role of PCA in the emergence of leaf epinasty and root growth anomalies, and be directed to improve our understanding of the molecular interactions of PCA in various fruit crops and cultivars.
Author Information
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- Michael Oberhuber - Laimburg Research Centre, Laimburg 6, Pfatten (Vadena), IT-39040 Auer (Ora), South Tyrol, Italy;
http://orcid.org/0000-0002-9989-7297;
The Laimburg Research Centre is funded by the Autonomous Province of Bozen-Bolzano.
Acknowledgments
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Josef Terleth, Andrea Furlato, Carlo Spolaore, and Stephan Raffl are gratefully acknowledged for technical assistance.
| SI | symptom index |
| PCA | 3-chloro-5-trifluoromethylpyridine-2-carboxylic acid |
| LC–MS | liquid chromatography–mass spectrometry |
| BBCH | Biologische Bundesanstalt, Bundessortenamt and Chemische Industrie |
| IAA | indole-3-acetic acid |
| ABP1 | auxin binding protein |
| TIR1 | transport inhibitor response |
| FW | fresh weight |
| nd | not detected |
| na | not available |
| asl | above sea level |
| ai | active ingredient |
References
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This article references 29 other publications.
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- 7McManus, P. S.; Kartanos, V.; Stasiak, M. Sensitivity of cold-climate wine grape cultivars to copper, sulfur, and difenoconazole fungicides. Crop Prot. 2017, 92, 122– 130, DOI: 10.1016/j.cropro.2016.10.027Google Scholar7https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XhvVWmtbbN&md5=a53f5e764d900d094663e9ce71d874fcSensitivity of cold-climate wine grape cultivars to copper, sulfur, and difenoconazole fungicidesMcManus, Patricia S.; Kartanos, Victoria; Stasiak, MattCrop Protection (2017), 92 (), 122-130CODEN: CRPTD6; ISSN:0261-2194. (Elsevier Ltd.)The development of wine grape cultivars that can withstand temps. as low as -40 °C, hereafter referred to as cold-climate cultivars, has been crit. to the establishment and growth of the wine industry in the northern USA. While some grape cultivars are susceptible to leaf injury following application of copper, sulfur, and difenoconazole fungicides, the sensitivity of most cold-climate cultivars to these fungicides is not known. In field trials conducted over four years at two locations in Wisconsin, USA, we found that most of the 15 cold-climate cultivars evaluated were not highly sensitive to copper, sulfur, or difenoconazole, although there were important exceptions. Sensitivity was expressed in relative terms, with comparisons made among the cultivars tested, and more wt. given when injury was obsd. after a small no. of applications. Regarding copper: Brianna was highly sensitive, showing injury in seven of 11 trials, sometimes after three or fewer applications; Le´on Millot, and Mare´chal Foch were moderately sensitive, each showing injury in three of six trials; and Frontenac, Frontenac gris, La Crescent, Marquette, and St. Croix were slightly sensitive, each showing injury in one or two trials. Regarding sulfur: Brianna, Le´on Millot, and Mare´chal Foch were highly sensitive, each showing injury in three trials, sometimes after three or fewer applications; and La Crescent and St. Croix were slightly sensitive, each showing injury in one trial. With the exception of Noiret, which showed injury in one trial, none of the cultivars was sensitive to difenoconazole. It should be possible for growers to integrate these fungicides into disease management programs that will control important diseases of wine grape and delay the emergence of pathogens resistant to major classes of synthetic fungicides.
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- 15Grossmann, K. Mediation of herbicide effects by hormone interactions. J. Plant Growth Regul. 2003, 22 (1), 109– 122, DOI: 10.1007/s00344-003-0020-0Google Scholar14https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD3sXosF2kurs%253D&md5=143d675a9ab2faa16c67318c6034f5f6Mediation of herbicide effects by hormone interactionsGrossmann, KlausJournal of Plant Growth Regulation (2003), 22 (1), 109-122CODEN: JPGRDI; ISSN:0721-7595. (Springer-Verlag New York Inc.)A review. Chem. manipulation of the phytohormone system involves the use of herbicides for weed control in modern crop prodn. In the latter case, only compds. interacting with the auxin system have gained practical importance. Auxin herbicides mimic the overdose effects of IAA, the principal natural auxin in higher plants. With their ability to control, particularly, dicotyledonous weeds in cereal crops, the synthetic auxins have been among the most successful herbicides used in agriculture. A newly discovered sequential hormone interaction plays a decisive role in their mode of action. The induction of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase in ethylene biosynthesis is the primary target process, following auxin herbicide signalling. Although the exact mol. target site has yet to be identified, it appears likely to be at the level of auxin receptor(s) for perception or signalling, leading ultimately to species- and organ-specific de novo enzyme synthesis. In sensitive dicots, ethylene causes epinastic growth and tissue swelling. Ethylene also triggers the biosynthesis of abscisic acid (ABA), mainly through the stimulated cleavage of xanthophylls to xanthoxal, catalyzed by 9-cis-epoxycarotenoid dioxygenase (NCED). ABA mediates stomatal closure which limits photosynthetic activity and biomass prodn., accompanied by an overprodn. of reactive oxygen species. Growth inhibition, senescence and tissue decay are the consequences. Recent results suggest that ethylene-triggered ABA is not restricted to the action of auxin herbicides. It may function as a module in the signalling of a variety of stimuli leading to plant growth regulation. An addnl. phenomenon is caused by the auxin herbicide quinclorac which also controls grass weeds. Here, quinclorac induces the accumulation of phytotoxic levels of cyanide, a co-product of ethylene, which ultimately derives from herbicide-induced ACC synthase activity in the tissue. Phytotropins are a further group of hormone-related compds. which are used as herbicides. They inhibit polar auxin transport by interacting with a regulatory protein, the NPA-binding protein, of the auxin efflux carrier. This causes an abnormal accumulation of IAA and applied synthetic auxins in plant meristems. Growth inhibition, loss of tropic responses and, in combination with auxin herbicides, synergistic effects are the consequences.
- 16Fedtke, C.; Duke, S. O. Herbicides. In Plant Toxicology, 4th ed.; Hock, B., Elstner, E. F., Eds.; Marcel Dekker: New York, 2005; pp 247– 330.Google ScholarThere is no corresponding record for this reference.
- 17Song, Y. Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. J. Integr. Plant Biol. 2014, 56 (2), 106– 113, DOI: 10.1111/jipb.12131Google Scholar16https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2cXmsFWqt7c%253D&md5=286a30ef05d6b34116d3645f23bbc8deInsight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicideSong, YalingJournal of Integrative Plant Biology (2014), 56 (2), 106-113CODEN: JIPBAV; ISSN:1672-9072. (Wiley-Blackwell)A review. 2,4-Dichlorophenoxyacetic acid (2,4-D) was the first synthetic herbicide to be com. developed and has commonly been used as a broadleaf herbicide for over 60 years. It is a selective herbicide that kills dicots without affecting monocots and mimics natural auxin at the mol. level. Physiol. responses of dicots sensitive to auxinic herbicides include abnormal growth, senescence, and plant death. The identification of auxin receptors, auxin transport carriers, transcription factors response to auxin, and cross-talk among phytohormones have shed light on the mol. action mode of 2,4-D as a herbicide. Here, the mol. action mode of 2,4-D is highlighted according to the latest findings, emphasizing the physiol. process, perception, and signal transduction under herbicide treatment.
- 18Grossmann, K. Auxin herbicides: Current status of mechanismandmode of action. Pest Manage. Sci. 2010, 66, 113– 120, DOI: 10.1002/ps.1860Google Scholar17https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3cXjvVSktA%253D%253D&md5=0fe7c250f45656c0a12c38204c6494bcAuxin herbicides: current status of mechanism and mode of actionGrossmann, KlausPest Management Science (2010), 66 (2), 113-120CODEN: PMSCFC; ISSN:1526-498X. (John Wiley & Sons Ltd.)A review. Synthetic compds. that act like phytohormonal superauxins have been among the most successful herbicides used in agriculture for >60 yr. These so-called auxin herbicides are more stable in planta than the main natural auxin, indole-3-acetic acid (IAA), and show systemic mobility and selective action, preferentially against dicot weeds in cereal crops. They belong to different chem. classes, which include phenoxycarboxylic acids, benzoic acids, pyridinecarboxylic acids, arom. carboxymethyl derivs., and quinolinecarboxylic acids. The recent identification of receptors for auxin perception and the discovery of a new hormone interaction in signaling between auxin, ethylene, and the upregulation of abscisic acid biosynthesis account for a large part of the repertoire of auxin-herbicide-mediated responses, which include growth inhibition, senescence, and tissue decay in sensitive dicots. An addnl. phenomenon is caused by the quinolinecarboxylic acid quinclorac, which also controls grass weeds. The accumulation of phytotoxic levels of tissue cyanide, derived ultimately from quinclorac-stimulated ethylene biosynthesis, plays a key role in eliciting the herbicidal symptoms in sensitive grasses. Copyright © 2009 Society of Chem. Industry.
- 19Mangin, A. R.; Hall, L. M. First report: Spotted knapweed (Centaurea stoebe) resistance to auxinic herbicides. Can. J. Plant Sci. 2016, 96 (6), 928– 931, DOI: 10.1139/cjps-2016-0008Google Scholar18https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2sXhsFeiu7%252FO&md5=537570c687306fa55ccfc2ef0b0cc6b5First report: spotted knapweed (Centaurea stoebe) resistance to auxinic herbicidesMangin, Amy R.; Hall, Linda M.Canadian Journal of Plant Science (2016), 96 (6), 928-931CODEN: CPLSAY; ISSN:0008-4220. (Canadian Science Publishing)Spotted knapweed is a prohibited noxious weed that is primarily controlled with auxinic herbicides. A population collected from a managed rangeland in East Kootenay, BC, was highly resistant to both clopyralid and picloram, with R/S ratios of >25 600 and 28, resp. This is the first report of resistance in spotted knapweed.
- 20Christoffoleti, P. J.; Alves de Figueiredo, M. R.; Pereira Peres, L. E.; Nissen, S.; Gaines, T. Auxinic herbicides, mechanisms of action, and weed resistance: A look into recent plant science advances. Sci. Agric. 2015, 72 (4), 356– 362, DOI: 10.1590/0103-9016-2014-0360Google Scholar19https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XhtlejtLnM&md5=6ce07bcc9a5900555df83887a7bb74b9Auxinic herbicides, mechanisms of action, and weed resistance: A Iook into recent plant science advancesChristoffoleti, Pedro Jacob; Alves de Figueiredo, Marcelo Rodrigues; Peres, Lazaro Eustaquio Pereira; Nissen, Scott; Gaines, ToddScientia Agricola (Piracicaba, Brazil) (2015), 72 (4), 356-362CODEN: SGRIEF; ISSN:0103-9016. (USP/ESALQ)Auxin governs dynamic cellular processes involved at several stages of plant growth and development. In this review, we discuss the mechanisms employed by auxin in light of recent scientific advances, with a focus on synthetic auxins as herbicides and synthetic auxin resistance mechanisms. Two auxin receptors were reported. The plasma membrane receptor ABP1 Auxin Binding Protein (1) alters the structure and arrangement of actin filaments and microtubules, leading to plant epinasty and reducing peroxisomes and mitochondria mobility in the cell environment. The second auxin receptor is the gene transcription pathway regulated by the SCTir/AFB ubiquitination complex, which destroys transcription repressor proteins that interrupt Auxin Response Factor (ARF) activation. As a result mRNA related with Abscisic Acid (ABA) and ethylene are transcribed, producing high quantities of theses hormones. Their assocd. action leads to high prodn. of Reactive Oxygen Species (ROS), leading to tissue and plant death. Recently, another ubiquitination pathway which is described as a new auxin signaling route is the F-box protein S-Phase Kinase-Assocd. Protein 2A (SKP2A). It is active in cell division regulation and there is evidence that auxin herbicides can deregulate the SKP2A pathway, which leads to severe defects in plant development. In this discussion, we propose that SFCSKP2A auxin binding site alteration could be a new auxinic herbicide resistance mechanism, a concept which may contribute to the current progress in plant biol. in its quest to clarify the many questions that still surround auxin herbicide mechanisms of action and the mechanisms of weed resistance.
- 21Woodward, A. W.; Bartel, B. Auxin: Regulation, action, and interaction. Ann. Bot. 2005, 95 (5), 707– 735, DOI: 10.1093/aob/mci083Google Scholar20https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXjvFOrsbs%253D&md5=e9c6c690fe7f0db1e9828f6ecca508dcAuxin: Regulation, action, and interactionWoodward, Andrew W.; Bartel, BonnieAnnals of Botany (Oxford, United Kingdom) (2005), 95 (5), 707-735CODEN: ANBOA4; ISSN:0305-7364. (Oxford University Press)A review. The phytohormone auxin is crit. for plant growth and orchestrates many developmental processes. This review considers the complex array of mechanisms plants use to control auxin levels, the movement of auxin through the plant, the emerging view of auxin-signalling mechanisms, and several interactions between auxin and other phytohormones. Though many natural and synthetic compds. exhibit auxin-like activity in bioassays, indole-3-acetic acid (IAA) is recognized as the key auxin in most plants. IAA is synthesized both from tryptophan (Trp) using Trp-dependent pathways and from an indolic Trp precursor via Trp-independent pathways; none of these pathways is fully elucidated. Plants can also obtain IAA by β-oxidn. of indole-3-butyric acid (IBA), a second endogenous auxin, or by hydrolyzing IAA conjugates, in which IAA is linked to amino acids, sugars or peptides. To permanently inactivate IAA, plants can employ conjugation and direct oxidn. Consistent with its definition as a hormone, IAA can be transported the length of the plant from the shoot to the root; this transport is necessary for normal development, and more localized transport is needed for tropic responses. Auxin signalling is mediated, at least in large part, by an SCFTIR1 E3 ubiquitin ligase complex that accelerates Aux/IAA repressor degrdn. in response to IAA, thereby altering gene expression. Two classes of auxin-induced genes encode neg. acting products (the Aux/IAA transcriptional repressors and GH3 family of IAA conjugating enzymes), suggesting that timely termination of the auxin signal is crucial. Auxin interaction with other hormone signals adds further challenges to understanding auxin response. Nearly six decades after the structural elucidation of IAA, many aspects of auxin metab., transport and signalling are well established; however, more than a few fundamental questions and innumerable details remain unresolved.
- 22Vanneste, S.; Friml, J. Auxin: A trigger for change in plant development. Cell 2009, 136 (6), 1005– 1016, DOI: 10.1016/j.cell.2009.03.001Google Scholar21https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1MXltFSntro%253D&md5=d4daced3a1dddb7c85e7a3d3c3af1eacAuxin: a trigger for change in plant developmentVanneste, Steffen; Friml, JiriCell (Cambridge, MA, United States) (2009), 136 (6), 1005-1016CODEN: CELLB5; ISSN:0092-8674. (Cell Press)A review with commentary. The dynamic, differential distribution of the hormone auxin within plant tissues controls an impressive variety of developmental processes, which tailor plant growth and morphol. to environmental conditions. Various environmental and endogenous signals can be integrated into changes in auxin distribution through their effects on local auxin biosynthesis and intercellular auxin transport. Individual cells interpret auxin largely by a nuclear signaling pathway that involves the F box protein TIR1 acting as an auxin receptor. Auxin-dependent TIR1 activity leads to ubiquitination-based degrdn. of transcriptional repressors and complex transcriptional reprogramming. Thus, auxin appears to be a versatile trigger of preprogrammed developmental changes in plant cells.
- 23Kelley, K. B.; Riechers, D. E. Recent developments in auxin biology and new opportunities for auxinic herbicide research. Pestic. Biochem. Physiol. 2007, 89 (1), 1– 11, DOI: 10.1016/j.pestbp.2007.04.002Google Scholar22https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2sXotValtrw%253D&md5=4b887f6a53cf8d1ccd3a59685fb3515aRecent developments in auxin biology and new opportunities for auxinic herbicide researchKelley, Kevin B.; Riechers, Dean E.Pesticide Biochemistry and Physiology (2007), 89 (1), 1-11CODEN: PCBPBS; ISSN:0048-3575. (Elsevier B.V.)A review. Auxinic herbicides mimic the effects of natural auxin. However, in spite of decades of research, the site(s) of action of auxinic herbicides has remained unknown and many physiol. aspects of their function are unclear. Recent advances in auxin biol. provide new opportunities for research into the mode of action of auxinic herbicides. Of considerable interest is the discovery of auxin receptors (TIR1 and possibly ABP1) that may lead to the discovery of auxinic herbicide site(s) of action. Knowledge of auxin-conjugating enzymes and auxin signal transduction components may shed new light on herbicide activity, selectivity in dicots, and mechanisms leading to phytotoxicity in sensitive plants. Anal. of genes induced in response to auxin may provide a novel approach for detection of off-target herbicide injury in crops. For example, the auxin-responsive gene GH3 is highly and specifically induced in response to auxinic herbicides in soybean, and may offer a novel method for diagnosing auxinic herbicide injury. Advances in the understanding of auxin biol. will provide many new avenues and opportunities for auxinic herbicide research in the future.
- 24Dharmasiri, N.; Dharmasiri, S.; Estelle, M. The F-box protein TIR1 is anauxin receptor. Nature 2005, 435, 441– 445, DOI: 10.1038/nature03543Google Scholar23https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXksVeisrs%253D&md5=db87d9696f0bdb7003b79a7a95ab32d8The F-box protein TIR1 is an auxin receptorDharmasiri, Nihal; Dharmasiri, Sunethra; Estelle, MarkNature (London, United Kingdom) (2005), 435 (7041), 441-445CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)The plant hormone auxin regulates diverse aspects of plant growth and development. Recent studies indicate that auxin acts by promoting the degrdn. of the Aux/IAA transcriptional repressors through the action of the ubiquitin protein ligase SCFTIR1. The nature of the signalling cascade that leads to this effect is not known. However, recent studies indicate that the auxin receptor and other signalling components involved in this response are sol. factors. Using an in vitro pull-down assay, we demonstrate that the interaction between transport inhibitor response 1 (TIR1) and Aux/IAA proteins does not require stable modification of either protein. Instead auxin promotes the Aux/IAA-SCFTIR1 interaction by binding directly to SCFTIR1. We further show that the loss of TIR1 and three related F-box proteins eliminates saturable auxin binding in plant exts. Finally, TIR1 synthesized in insect cells binds Aux/IAA proteins in an auxin-dependent manner. Together, these results indicate that TIR1 is an auxin receptor that mediates Aux/IAA degrdn. and auxin-regulated transcription.
- 25Dharmasiri, N.; Dharmasiri, S.; Weijers, D.; Lechner, E.; Yamada, M.; Hobbie, L.; Ehrismann, J. S.; Jürgens, G.; Estelle, M. Plant development is regulated by a family of auxin receptorF box proteins. Dev. Cell 2005, 9, 109– 119, DOI: 10.1016/j.devcel.2005.05.014Google Scholar24https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXmvVehurg%253D&md5=7db106eb1b509dc80d53b6a69da06a03Plant development is regulated by a family of auxin receptor F box proteinsDharmasiri, Nihal; Dharmasiri, Sunethra; Weijers, Dolf; Lechner, Esther; Yamada, Masashi; Hobbie, Lawrence; Ehrismann, Jasmin S.; Juergens, Gerd; Estelle, MarkDevelopmental Cell (2005), 9 (1), 109-119CODEN: DCEEBE; ISSN:1534-5807. (Cell Press)The plant hormone auxin has been implicated in virtually every aspect of plant growth and development. Auxin acts by promoting the degrdn. of transcriptional regulators called Aux/IAA proteins. Aux/IAA degrdn. requires TIR1, an F box protein that has been shown to function as an auxin receptor. However, loss of TIR1 has a modest effect on auxin response and plant development. Here we show that three addnl. F box proteins, called AFB1, 2, and 3, also regulate auxin response. Like TIR1, these proteins interact with the Aux/IAA proteins in an auxin-dependent manner. Plants that are deficient in all four proteins are auxin insensitive and exhibit a severe embryonic phenotype similar to the mp/arf5 and bdl/iaa12 mutants. Correspondingly, all TIR1/AFB proteins interact with BDL, and BDL is stabilized in triple mutant plants. Our results indicate that TIR1 and the AFB proteins collectively mediate auxin responses throughout plant development.
- 26Kepinski, S.; Leyser, O. The Arabidopsis TIR1 protein is an auxinreceptor. Nature 2005, 435, 446– 451, DOI: 10.1038/nature03542Google Scholar25https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXksVeisro%253D&md5=5b678dcd5c5c88a23b7d0815be915dfaThe Arabidopsis F-box protein TIR1 is an auxin receptorKepinski, Stefan; Leyser, OttolineNature (London, United Kingdom) (2005), 435 (7041), 446-451CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)Despite 100 years of evidence showing a pivotal role for indole-3-acetic acid (IAA or auxin) in plant development, the mechanism of auxin perception has remained elusive. Central to auxin response are changes in gene expression, brought about by auxin-induced interaction between the Aux/IAA transcriptional repressor proteins and the ubiquitin-ligase complex SCFTIR1, thus targeting for them proteolysis. Regulated SCF-mediated protein degrdn. is a widely occurring signal transduction mechanism. Target specificity is conferred by the F-box protein subunit of the SCF (TIR1 in the case of Aux/IAAs) and there are multiple F-box protein genes in all eukaryotic genomes examd. so far. Although SCF-target interaction is usually regulated by signal-induced modification of the target, we have previously shown that auxin signalling involves the modification of SCFTIR1. Here we show that this modification involves the direct binding of auxin to TIR1 and thus that TIR1 is an auxin receptor mediating transcriptional responses to auxin.
- 27Tan, X.; Calderon-Villalobos, L. I. A.; Sharon, M.; Zheng, C.; Robinson, C. V.; Estelle, M.; Zheng, N. Mechanism of auxinperceptionby the TIR1 ubiquitinligase. Nature 2007, 446, 640– 645, DOI: 10.1038/nature05731Google Scholar26https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2sXjslOlsbc%253D&md5=cbf2367ed117aeb6b1cc6e6e85f36605Mechanism of auxin perception by the TIR1 ubiquitin ligaseTan, Xu; Calderon-Villalobos, Luz Irina A.; Sharon, Michal; Zheng, Changxue; Robinson, Carol V.; Estelle, Mark; Zheng, NingNature (London, United Kingdom) (2007), 446 (7136), 640-645CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)Auxin is a pivotal plant hormone that controls many aspects of plant growth and development. The major naturally occurring auxin, indole-3-acetic acid (IAA), coordinates many plant growth processes by modulating gene expression, which leads to changes in cell division, elongation, and differentiation. Perceived by a small family of F-box proteins including transport inhibitor response 1 (TIR1), auxin regulates gene expression by promoting SCF ubiquitin-ligase-catalyzed degrdn. of the Aux/IAA transcription repressors, but how the TIR1 F-box protein senses and becomes activated by auxin remains unclear. Here we present the crystal structures of the Arabidopsis TIR1-ASK1 complex in ligand-free form and in complexes with three different auxin compds. and an Aux/IAA substrate peptide. These structures show that the leucine-rich repeat (LRR) domain of TIR1 contains an unexpected inositol hexakisphosphate (InsP6) co-factor and recognizes auxin and the Aux/IAA polypeptide substrate through a single surface pocket. Anchored to the base of the TIR1 pocket, auxin binds to a partially promiscuous site, which can also accommodate various auxin analogs. Docked on top of auxin, the Aux/IAA substrate peptide occupies the rest of the TIR1 pocket and completely encloses the hormone-binding site. By filling in a hydrophobic cavity at the protein interface, auxin enhances the TIR1-substrate interactions by acting as a 'mol. glue'. Our results establish the first structural model of a plant hormone receptor.
- 28European Food Safety Authority (EFSA). Draft Assessment Report Fluopyram; EFSA: Parma, Italy, Aug 15, 2011; Vol. 3, Annex B, B.7 Residue Data, pp 23– 24, http://dar.efsa.europa.eu/dar-web/provision (accessed Aug 31, 2018).Google ScholarThere is no corresponding record for this reference.
- 29Keller, M. Phenology and Growth Cycle. In The Science of Grapevines Anatomy and Physiology, 2nd ed.; Academic Press: Cambridge, MA, 2015.Google ScholarThere is no corresponding record for this reference.
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Abstract
Figure 1
Figure 1. Constitutional formulas of fluopyram and fluopicolide and metabolites of fluopyram in V. vinifera leaves (left) and formula of the herbicide clopyralid (bottom right). Fluopyram-8-OH, N-{2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-1-hydroxyethyl}-2-(trifluoromethyl)benzamide; fluopyram-7-OH, N-{2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-2-hydroxyethyl}-2-(trifluoromethyl)benzamide; and fluopyram-7-OGlc, N-[2-[3-chloro-5-(trifluoromethyl)pyridin-2-yl]-2-(β-glucopyranosyloxy)ethyl]-2-(trifluoromethyl)benzamide (fluopyram numbering according to ref (9)).
Figure 2
Figure 2. Growth distortion symptoms on V. vinifera flowers and leaves. (Left) Leaf symptom index (SI; 0, asymptomatic/no distortion (not shown); 1, light; 2, intermediate; and 3, strong distortion on leaves) and grape symptom index (SI; 0, no loss of berries in grape clusters (not shown); 1, 1–33% loss; 2, 33–66% loss; and 3, 66–100% loss), (center) symptomatic leaves from fluopyram-treated commercial vineyards (i) and symptoms on new grown leaves after PCA treatment (ii), and (right) symptomatic grapes from fluopyram-treated commercial vineyards (iii). Pictures of grapes SI 1 and 2 are at phenology stage BBCH = 73, and grapes SI 3 and affected grapes from commercial fields (iii) are at phenology stage BBCH = 71–73.
Figure 3
Figure 4
Figure 4. Root development of potted vines cv. Gewürztraminer after foliar treatment with 0.02% PCA (left) and control plants (right).
References
This article references 29 other publications.
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- 2Gessler, C.; Pertot, I.; Perazzolli, M. Plasmoparaviticola: A review of knowledge on downy mildew of grapevine and effective disease management. Phytopathol. Mediterr. 2011, 50, 3– 44, DOI: 10.14601/Phytopathol_Mediterr-9360There is no corresponding record for this reference.
- 3Glawe, D. A. The powdery mildews: A review of the world’s most familiar (yet poorly known) plant pathogens. Annu. Rev. Phytopathol. 2008, 46, 27– 51, DOI: 10.1146/annurev.phyto.46.081407.1047403https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1cXhtFCqt77I&md5=04a5ed1b9e6d5ad1304f0d9ca8911375The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogensGlawe, Dean A.Annual Review of Phytopathology (2008), 46 (), 27-51CODEN: APPYAG; ISSN:0066-4286. (Annual Reviews Inc.)A review. The past decade has seen fundamental changes in our understanding of powdery mildews (Erysiphales). Research on mol. phylogeny demonstrated that Erysiphales are Leotiomycetes (inoperculate discomycetes) rather than Pyrenomycetes or Plectomycetes. Life cycles are surprisingly variable, including both sexual and asexual states, or only sexual states, or only asexual states. At least one species produces dematiaceous conidia. Analyses of rDNA sequences indicate that major lineages are more closely correlated with anamorphic features such as conidial ontogeny and morphol. than with teleomorph features. Development of mol. clock models is enabling researchers to reconstruct patterns of coevolution and host-jumping, as well as ancient migration patterns. Geog. distributions of some species appear to be increasing rapidly but little is known about species diversity in many large areas, including North America. Powdery mildews may already be responding to climate change, suggesting they may be useful models for studying effects of climate change on plant diseases.
- 4Williamson, B.; Tudzynski, B.; Tudzynski, P.; van Kan, J. A. L. Botrytis cinerea: The cause of grey mould disease. Mol. Plant Pathol. 2007, 8 (5), 561– 580, DOI: 10.1111/j.1364-3703.2007.00417.x4https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2sXhtV2murzP&md5=8b6ee2075e9b485d0cbafd8f27c6bb5fBotrytis cinerea: the cause of grey mould diseaseWilliamson, Brian; Tudzynski, Bettina; Tudzynski, Paul; Van Kan, Jan A. L.Molecular Plant Pathology (2007), 8 (5), 561-580CODEN: MPPAFD; ISSN:1464-6722. (Blackwell Publishing Ltd.)A review. Botrytis cinerea (teleomorph: Botryotinia fuckeliana) is an airborne plant pathogen with a necrotrophic lifestyle attacking over 200 crop hosts worldwide. Although there are fungicides for its control, many classes of fungicides have failed due to its genetic plasticity. It has become an important model for mol. study of necrotrophic fungi. Kingdom: Fungi, phylum: Ascomycota, subphylum: Pezizomycotina, class: Leotiomycetes, order: Helotiales, family: Sclerotiniaceae, genus: Botryotinia. Host range and symptoms: Over 200 mainly dicotyledonous plant species, including important protein, oil, fiber and horticultural crops, are affected in temperate and subtropical regions. It can cause soft rotting of all aerial plant parts, and rotting of vegetables, fruits and flowers post-harvest to produce prolific gray conidiophores and (macro)conidia typical of the disease. B. cinerea produces a range of cell-well-degrading enzymes, toxins and other two-mol.-wt. compds. such as oxalic acid. New evidence suggests that the pathogen triggers the host to induce programmed cell death as an attack strategy. There are few examples of robust genetic host resistance, but recent work has identified quant. trait loci in tomato that offer new approaches for stable polygenic resistance in future.
- 5Casida, J. Pesticide interactions: Mechanisms, benefits, and risks. J. Agric. Food Chem. 2017, 65 (23), 4553– 4561, DOI: 10.1021/acs.jafc.7b018135https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2sXotlSku70%253D&md5=e979e8961c04d607eeeda0a578b50819Pesticide Interactions: Mechanisms, Benefits, and RisksCasida, John E.Journal of Agricultural and Food Chemistry (2017), 65 (23), 4553-4561CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)A review. Interactions between pesticides at common mol. targets and detoxification systems often det. their effectiveness and safety. Compds. with the same mode of action or target are candidates for cross resistance and restrictions in their recommended uses. Discovery research is therefore focused on new mechanisms and modes of action. Interactions in detoxification systems also provide cross resistance and synergist and safener mechanisms illustrated with serine hydrolases and inhibitors, cytochrome P 450 and insecticide synergists, and glutathione S-transferases and herbicide safeners. Secondary targets are also considered for inhibitors of serine hydrolases, aldehyde dehydrogenases, and transporters. Emphasis is given to the mechanistic aspects of interactions, not the incidence, which depends on potency, exposure, ratios, and timing. The benefits of pesticide interactions are the addnl. levels of chem. control to achieve desired organismal effects. The risks are the unpredictable interactions of complex interconnected biol. systems. However, with care, two can be better than one.
- 6Petit, A.-N.; Fontaine, F.; Vatsa, P.; Clement, C.; Vaillant-Gaveau, N. Fungicide impacts on photosynthesis in crop plants. Photosynth. Res. 2012, 111 (3), 315– 326, DOI: 10.1007/s11120-012-9719-86https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC38Xjs1CqsLc%253D&md5=cee55e78a68ebada808c94a98e806353Fungicide impacts on photosynthesis in crop plantsPetit, Anne-Noelle; Fontaine, Florence; Vatsa, Parul; Clement, Christophe; Vaillant-Gaveau, NathaliePhotosynthesis Research (2012), 111 (3), 315-326CODEN: PHRSDI; ISSN:0166-8595. (Springer)A review. Fungicides are widely used to control pests in crop plants. However, it was reported that these pesticides may have neg. effects on crop physiol., esp. on photosynthesis. An alteration in photosynthesis might lead to a redn. in photoassimilate prodn., resulting in a decrease in both growth and yield of crop plants. For example, a contact fungicide such as Cu inhibits photosynthesis by destroying chloroplasts, affecting photosystem II activity and chlorophyll biosynthesis. Systemic fungicides such as benzimidazoles, anilides, and pyrimidine are also phytotoxic, whereas azoles stimulate photosynthesis. This article focuses on the available information about toxic effects of fungicides on photosynthesis in crop plants, highlighting the mechanisms of perturbation, interaction, and the target sites of different classes of fungicides.
- 7McManus, P. S.; Kartanos, V.; Stasiak, M. Sensitivity of cold-climate wine grape cultivars to copper, sulfur, and difenoconazole fungicides. Crop Prot. 2017, 92, 122– 130, DOI: 10.1016/j.cropro.2016.10.0277https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XhvVWmtbbN&md5=a53f5e764d900d094663e9ce71d874fcSensitivity of cold-climate wine grape cultivars to copper, sulfur, and difenoconazole fungicidesMcManus, Patricia S.; Kartanos, Victoria; Stasiak, MattCrop Protection (2017), 92 (), 122-130CODEN: CRPTD6; ISSN:0261-2194. (Elsevier Ltd.)The development of wine grape cultivars that can withstand temps. as low as -40 °C, hereafter referred to as cold-climate cultivars, has been crit. to the establishment and growth of the wine industry in the northern USA. While some grape cultivars are susceptible to leaf injury following application of copper, sulfur, and difenoconazole fungicides, the sensitivity of most cold-climate cultivars to these fungicides is not known. In field trials conducted over four years at two locations in Wisconsin, USA, we found that most of the 15 cold-climate cultivars evaluated were not highly sensitive to copper, sulfur, or difenoconazole, although there were important exceptions. Sensitivity was expressed in relative terms, with comparisons made among the cultivars tested, and more wt. given when injury was obsd. after a small no. of applications. Regarding copper: Brianna was highly sensitive, showing injury in seven of 11 trials, sometimes after three or fewer applications; Le´on Millot, and Mare´chal Foch were moderately sensitive, each showing injury in three of six trials; and Frontenac, Frontenac gris, La Crescent, Marquette, and St. Croix were slightly sensitive, each showing injury in one or two trials. Regarding sulfur: Brianna, Le´on Millot, and Mare´chal Foch were highly sensitive, each showing injury in three trials, sometimes after three or fewer applications; and La Crescent and St. Croix were slightly sensitive, each showing injury in one trial. With the exception of Noiret, which showed injury in one trial, none of the cultivars was sensitive to difenoconazole. It should be possible for growers to integrate these fungicides into disease management programs that will control important diseases of wine grape and delay the emergence of pathogens resistant to major classes of synthetic fungicides.
- 8Palmer, J. W.; Davies, S. B.; Shaw, P. W.; Wunsche, J. N. Growth and fruit quality of ‘Braeburn’ apple (Malus domestica) trees as influenced by fungicide programmes suitable for organic production. N. Z. J. Crop Hortic. Sci. 2003, 31 (2), 169– 177, DOI: 10.1080/01140671.2003.95142498https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD3sXnsVCqt70%253D&md5=844687afa71d4480305cb597971993fcGrowth and fruit quality of "Braeburn" apple (Malus domestica) trees as influenced by fungicide programmes suitable for organic productionPalmer, J. W.; Davies, S. B.; Shaw, P. W.; Wuensche, J. N.New Zealand Journal of Crop and Horticultural Science (2003), 31 (2), 169-177CODEN: NZJSEF; ISSN:0114-0671. (RSNZ Publishing)Org. pipfruit growers in New Zealand have reported decreased yield and fruit size and poorer quality of foliage of "Braeburn" apple (Malus domestica) with fungicidal programs based on sulfur. This project aimed to quantify the effect of several fungicide programs compatible with org. prodn. on the tree growth, yield, and fruit quality of "Braeburn". The spray programs included Kocide DF, lime sulfur, Kumulus, slaked lime, Kocide DF + slaked lime, and Kocide DF + Kumulus compared to an Integrated Fruit Prodn. (IFP) compatible program based on dodine, polyram, and captan. The spray programs were applied from pink tip until harvest, with a total 19 spray applications made to 5-yr-old "Braeburn"/MM.106 trees. Spray treatments did not influence shoot growth, leaf area development, or increment in trunk cross-sectional area. Leaf photosynthesis was significantly reduced by all treatments which included sulfur (lime sulfur or Kumulus) with redns. of up to almost 50% in Jan. compared to the non-sulfur treatments. At harvest, the pooled data for the treatments contg. sulfur showed a significant yield per tree redn. of 12% compared to the non-sulfur treatments, largely as a result of decreased fruit nos. per tree. Treatments contg. Kocide DF resulted in a higher proportion of fruit with russet. The addn. of Kumulus or slaked lime to Kocide DF resulted in some amelioration of russet. All treatments resulted in less blush development on the fruit compared to the IFP control, except for slaked lime. Slaked lime treatments, however, tended to reduce sunburn. The Kocide DF + Kumulus treatment produced the highest reject rate for low color. Black spot (Venturia inaequalis) incidence on fruit at harvest was significantly higher on trees treated with either Kocide DF or slaked lime compared to the control treatment. When Kocide DF and slaked lime were used together, however, control of black spot was not significantly different from the control. In contrast, dry eye rot (Botrytis cinerea) incidence was significantly higher on the trees treated with lime sulfur.
- 9European Food Safety Authority (EFSA) Setting of new MRLs and import tolerances for fluopyram in various crops. EFSA J. 2011, 9 (9), 2388– 2455, DOI: 10.2903/j.efsa.2011.2388There is no corresponding record for this reference.
- 10Weather Service. The Daily, Monthly and Annual Data of Representative Weather Stations in the Autonomous Province of Bozen; Weather Service: Bozen-Bolzano, Italy, 2018; http://weather.provinz.bz.it/historical-data.asp (accessed Sept 13, 2018).There is no corresponding record for this reference.
- 11Robatscher, P.; Eisenstecken, D.; Raifer, B.; Innerebner, G.; Pedri, U.; Oberhuber, M.; Hafner, H. Untersuchungen zu den Wuchs- und Blühstörungen im Weinbau 2015: Abbauprodukt des Fungizids Fluopyram (LUNA PRIVILIGE) als Ursache. In Deutsches Weinbaujahrbuch 2017; Stoll, M., Schultz, H.-R., Eds.; Ulmer: Stuttgart, Germany, 2017; Vol. 68, pp 125– 130, ISBN: 978-3-8001-0863-3.There is no corresponding record for this reference.
- 12European Food Safety Authority (EFSA). Draft Assessment Report Fluopicolide; EFSA: Parma, Italy, Nov, 1, 2005; Vol. 3, Annex B, B.7. Residue Data, p 552, http://dar.efsa.europa.eu/dar-web/provision (accessed Aug 31, 2018).There is no corresponding record for this reference.
- 13Cobb, A. H. Auxin-type herbicides. In Herbicides and Plant Physiology, 2nd ed.; Cobb, A. H., Reade, J. P. H., Eds.; Wiley-Blackwell: West Sussex, U.K., 2010; pp 133– 155.There is no corresponding record for this reference.
- 14Sterling, T. M.; Hall, C. Mechanism of action of natural auxins and the auxinicherbicides. In Herbicide Activity: Toxicology, Biochemistry and Molecular Biology, 1st ed.; Roe, R. M., Burton, J. D., Kuhr, R. J., Eds.; IOS Press: Amsterdam, Netherlands, 1997; pp 111– 141.There is no corresponding record for this reference.
- 15Grossmann, K. Mediation of herbicide effects by hormone interactions. J. Plant Growth Regul. 2003, 22 (1), 109– 122, DOI: 10.1007/s00344-003-0020-014https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD3sXosF2kurs%253D&md5=143d675a9ab2faa16c67318c6034f5f6Mediation of herbicide effects by hormone interactionsGrossmann, KlausJournal of Plant Growth Regulation (2003), 22 (1), 109-122CODEN: JPGRDI; ISSN:0721-7595. (Springer-Verlag New York Inc.)A review. Chem. manipulation of the phytohormone system involves the use of herbicides for weed control in modern crop prodn. In the latter case, only compds. interacting with the auxin system have gained practical importance. Auxin herbicides mimic the overdose effects of IAA, the principal natural auxin in higher plants. With their ability to control, particularly, dicotyledonous weeds in cereal crops, the synthetic auxins have been among the most successful herbicides used in agriculture. A newly discovered sequential hormone interaction plays a decisive role in their mode of action. The induction of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase in ethylene biosynthesis is the primary target process, following auxin herbicide signalling. Although the exact mol. target site has yet to be identified, it appears likely to be at the level of auxin receptor(s) for perception or signalling, leading ultimately to species- and organ-specific de novo enzyme synthesis. In sensitive dicots, ethylene causes epinastic growth and tissue swelling. Ethylene also triggers the biosynthesis of abscisic acid (ABA), mainly through the stimulated cleavage of xanthophylls to xanthoxal, catalyzed by 9-cis-epoxycarotenoid dioxygenase (NCED). ABA mediates stomatal closure which limits photosynthetic activity and biomass prodn., accompanied by an overprodn. of reactive oxygen species. Growth inhibition, senescence and tissue decay are the consequences. Recent results suggest that ethylene-triggered ABA is not restricted to the action of auxin herbicides. It may function as a module in the signalling of a variety of stimuli leading to plant growth regulation. An addnl. phenomenon is caused by the auxin herbicide quinclorac which also controls grass weeds. Here, quinclorac induces the accumulation of phytotoxic levels of cyanide, a co-product of ethylene, which ultimately derives from herbicide-induced ACC synthase activity in the tissue. Phytotropins are a further group of hormone-related compds. which are used as herbicides. They inhibit polar auxin transport by interacting with a regulatory protein, the NPA-binding protein, of the auxin efflux carrier. This causes an abnormal accumulation of IAA and applied synthetic auxins in plant meristems. Growth inhibition, loss of tropic responses and, in combination with auxin herbicides, synergistic effects are the consequences.
- 16Fedtke, C.; Duke, S. O. Herbicides. In Plant Toxicology, 4th ed.; Hock, B., Elstner, E. F., Eds.; Marcel Dekker: New York, 2005; pp 247– 330.There is no corresponding record for this reference.
- 17Song, Y. Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. J. Integr. Plant Biol. 2014, 56 (2), 106– 113, DOI: 10.1111/jipb.1213116https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2cXmsFWqt7c%253D&md5=286a30ef05d6b34116d3645f23bbc8deInsight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicideSong, YalingJournal of Integrative Plant Biology (2014), 56 (2), 106-113CODEN: JIPBAV; ISSN:1672-9072. (Wiley-Blackwell)A review. 2,4-Dichlorophenoxyacetic acid (2,4-D) was the first synthetic herbicide to be com. developed and has commonly been used as a broadleaf herbicide for over 60 years. It is a selective herbicide that kills dicots without affecting monocots and mimics natural auxin at the mol. level. Physiol. responses of dicots sensitive to auxinic herbicides include abnormal growth, senescence, and plant death. The identification of auxin receptors, auxin transport carriers, transcription factors response to auxin, and cross-talk among phytohormones have shed light on the mol. action mode of 2,4-D as a herbicide. Here, the mol. action mode of 2,4-D is highlighted according to the latest findings, emphasizing the physiol. process, perception, and signal transduction under herbicide treatment.
- 18Grossmann, K. Auxin herbicides: Current status of mechanismandmode of action. Pest Manage. Sci. 2010, 66, 113– 120, DOI: 10.1002/ps.186017https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3cXjvVSktA%253D%253D&md5=0fe7c250f45656c0a12c38204c6494bcAuxin herbicides: current status of mechanism and mode of actionGrossmann, KlausPest Management Science (2010), 66 (2), 113-120CODEN: PMSCFC; ISSN:1526-498X. (John Wiley & Sons Ltd.)A review. Synthetic compds. that act like phytohormonal superauxins have been among the most successful herbicides used in agriculture for >60 yr. These so-called auxin herbicides are more stable in planta than the main natural auxin, indole-3-acetic acid (IAA), and show systemic mobility and selective action, preferentially against dicot weeds in cereal crops. They belong to different chem. classes, which include phenoxycarboxylic acids, benzoic acids, pyridinecarboxylic acids, arom. carboxymethyl derivs., and quinolinecarboxylic acids. The recent identification of receptors for auxin perception and the discovery of a new hormone interaction in signaling between auxin, ethylene, and the upregulation of abscisic acid biosynthesis account for a large part of the repertoire of auxin-herbicide-mediated responses, which include growth inhibition, senescence, and tissue decay in sensitive dicots. An addnl. phenomenon is caused by the quinolinecarboxylic acid quinclorac, which also controls grass weeds. The accumulation of phytotoxic levels of tissue cyanide, derived ultimately from quinclorac-stimulated ethylene biosynthesis, plays a key role in eliciting the herbicidal symptoms in sensitive grasses. Copyright © 2009 Society of Chem. Industry.
- 19Mangin, A. R.; Hall, L. M. First report: Spotted knapweed (Centaurea stoebe) resistance to auxinic herbicides. Can. J. Plant Sci. 2016, 96 (6), 928– 931, DOI: 10.1139/cjps-2016-000818https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC2sXhsFeiu7%252FO&md5=537570c687306fa55ccfc2ef0b0cc6b5First report: spotted knapweed (Centaurea stoebe) resistance to auxinic herbicidesMangin, Amy R.; Hall, Linda M.Canadian Journal of Plant Science (2016), 96 (6), 928-931CODEN: CPLSAY; ISSN:0008-4220. (Canadian Science Publishing)Spotted knapweed is a prohibited noxious weed that is primarily controlled with auxinic herbicides. A population collected from a managed rangeland in East Kootenay, BC, was highly resistant to both clopyralid and picloram, with R/S ratios of >25 600 and 28, resp. This is the first report of resistance in spotted knapweed.
- 20Christoffoleti, P. J.; Alves de Figueiredo, M. R.; Pereira Peres, L. E.; Nissen, S.; Gaines, T. Auxinic herbicides, mechanisms of action, and weed resistance: A look into recent plant science advances. Sci. Agric. 2015, 72 (4), 356– 362, DOI: 10.1590/0103-9016-2014-036019https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC28XhtlejtLnM&md5=6ce07bcc9a5900555df83887a7bb74b9Auxinic herbicides, mechanisms of action, and weed resistance: A Iook into recent plant science advancesChristoffoleti, Pedro Jacob; Alves de Figueiredo, Marcelo Rodrigues; Peres, Lazaro Eustaquio Pereira; Nissen, Scott; Gaines, ToddScientia Agricola (Piracicaba, Brazil) (2015), 72 (4), 356-362CODEN: SGRIEF; ISSN:0103-9016. (USP/ESALQ)Auxin governs dynamic cellular processes involved at several stages of plant growth and development. In this review, we discuss the mechanisms employed by auxin in light of recent scientific advances, with a focus on synthetic auxins as herbicides and synthetic auxin resistance mechanisms. Two auxin receptors were reported. The plasma membrane receptor ABP1 Auxin Binding Protein (1) alters the structure and arrangement of actin filaments and microtubules, leading to plant epinasty and reducing peroxisomes and mitochondria mobility in the cell environment. The second auxin receptor is the gene transcription pathway regulated by the SCTir/AFB ubiquitination complex, which destroys transcription repressor proteins that interrupt Auxin Response Factor (ARF) activation. As a result mRNA related with Abscisic Acid (ABA) and ethylene are transcribed, producing high quantities of theses hormones. Their assocd. action leads to high prodn. of Reactive Oxygen Species (ROS), leading to tissue and plant death. Recently, another ubiquitination pathway which is described as a new auxin signaling route is the F-box protein S-Phase Kinase-Assocd. Protein 2A (SKP2A). It is active in cell division regulation and there is evidence that auxin herbicides can deregulate the SKP2A pathway, which leads to severe defects in plant development. In this discussion, we propose that SFCSKP2A auxin binding site alteration could be a new auxinic herbicide resistance mechanism, a concept which may contribute to the current progress in plant biol. in its quest to clarify the many questions that still surround auxin herbicide mechanisms of action and the mechanisms of weed resistance.
- 21Woodward, A. W.; Bartel, B. Auxin: Regulation, action, and interaction. Ann. Bot. 2005, 95 (5), 707– 735, DOI: 10.1093/aob/mci08320https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXjvFOrsbs%253D&md5=e9c6c690fe7f0db1e9828f6ecca508dcAuxin: Regulation, action, and interactionWoodward, Andrew W.; Bartel, BonnieAnnals of Botany (Oxford, United Kingdom) (2005), 95 (5), 707-735CODEN: ANBOA4; ISSN:0305-7364. (Oxford University Press)A review. The phytohormone auxin is crit. for plant growth and orchestrates many developmental processes. This review considers the complex array of mechanisms plants use to control auxin levels, the movement of auxin through the plant, the emerging view of auxin-signalling mechanisms, and several interactions between auxin and other phytohormones. Though many natural and synthetic compds. exhibit auxin-like activity in bioassays, indole-3-acetic acid (IAA) is recognized as the key auxin in most plants. IAA is synthesized both from tryptophan (Trp) using Trp-dependent pathways and from an indolic Trp precursor via Trp-independent pathways; none of these pathways is fully elucidated. Plants can also obtain IAA by β-oxidn. of indole-3-butyric acid (IBA), a second endogenous auxin, or by hydrolyzing IAA conjugates, in which IAA is linked to amino acids, sugars or peptides. To permanently inactivate IAA, plants can employ conjugation and direct oxidn. Consistent with its definition as a hormone, IAA can be transported the length of the plant from the shoot to the root; this transport is necessary for normal development, and more localized transport is needed for tropic responses. Auxin signalling is mediated, at least in large part, by an SCFTIR1 E3 ubiquitin ligase complex that accelerates Aux/IAA repressor degrdn. in response to IAA, thereby altering gene expression. Two classes of auxin-induced genes encode neg. acting products (the Aux/IAA transcriptional repressors and GH3 family of IAA conjugating enzymes), suggesting that timely termination of the auxin signal is crucial. Auxin interaction with other hormone signals adds further challenges to understanding auxin response. Nearly six decades after the structural elucidation of IAA, many aspects of auxin metab., transport and signalling are well established; however, more than a few fundamental questions and innumerable details remain unresolved.
- 22Vanneste, S.; Friml, J. Auxin: A trigger for change in plant development. Cell 2009, 136 (6), 1005– 1016, DOI: 10.1016/j.cell.2009.03.00121https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD1MXltFSntro%253D&md5=d4daced3a1dddb7c85e7a3d3c3af1eacAuxin: a trigger for change in plant developmentVanneste, Steffen; Friml, JiriCell (Cambridge, MA, United States) (2009), 136 (6), 1005-1016CODEN: CELLB5; ISSN:0092-8674. (Cell Press)A review with commentary. The dynamic, differential distribution of the hormone auxin within plant tissues controls an impressive variety of developmental processes, which tailor plant growth and morphol. to environmental conditions. Various environmental and endogenous signals can be integrated into changes in auxin distribution through their effects on local auxin biosynthesis and intercellular auxin transport. Individual cells interpret auxin largely by a nuclear signaling pathway that involves the F box protein TIR1 acting as an auxin receptor. Auxin-dependent TIR1 activity leads to ubiquitination-based degrdn. of transcriptional repressors and complex transcriptional reprogramming. Thus, auxin appears to be a versatile trigger of preprogrammed developmental changes in plant cells.
- 23Kelley, K. B.; Riechers, D. E. Recent developments in auxin biology and new opportunities for auxinic herbicide research. Pestic. Biochem. Physiol. 2007, 89 (1), 1– 11, DOI: 10.1016/j.pestbp.2007.04.00222https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2sXotValtrw%253D&md5=4b887f6a53cf8d1ccd3a59685fb3515aRecent developments in auxin biology and new opportunities for auxinic herbicide researchKelley, Kevin B.; Riechers, Dean E.Pesticide Biochemistry and Physiology (2007), 89 (1), 1-11CODEN: PCBPBS; ISSN:0048-3575. (Elsevier B.V.)A review. Auxinic herbicides mimic the effects of natural auxin. However, in spite of decades of research, the site(s) of action of auxinic herbicides has remained unknown and many physiol. aspects of their function are unclear. Recent advances in auxin biol. provide new opportunities for research into the mode of action of auxinic herbicides. Of considerable interest is the discovery of auxin receptors (TIR1 and possibly ABP1) that may lead to the discovery of auxinic herbicide site(s) of action. Knowledge of auxin-conjugating enzymes and auxin signal transduction components may shed new light on herbicide activity, selectivity in dicots, and mechanisms leading to phytotoxicity in sensitive plants. Anal. of genes induced in response to auxin may provide a novel approach for detection of off-target herbicide injury in crops. For example, the auxin-responsive gene GH3 is highly and specifically induced in response to auxinic herbicides in soybean, and may offer a novel method for diagnosing auxinic herbicide injury. Advances in the understanding of auxin biol. will provide many new avenues and opportunities for auxinic herbicide research in the future.
- 24Dharmasiri, N.; Dharmasiri, S.; Estelle, M. The F-box protein TIR1 is anauxin receptor. Nature 2005, 435, 441– 445, DOI: 10.1038/nature0354323https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXksVeisrs%253D&md5=db87d9696f0bdb7003b79a7a95ab32d8The F-box protein TIR1 is an auxin receptorDharmasiri, Nihal; Dharmasiri, Sunethra; Estelle, MarkNature (London, United Kingdom) (2005), 435 (7041), 441-445CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)The plant hormone auxin regulates diverse aspects of plant growth and development. Recent studies indicate that auxin acts by promoting the degrdn. of the Aux/IAA transcriptional repressors through the action of the ubiquitin protein ligase SCFTIR1. The nature of the signalling cascade that leads to this effect is not known. However, recent studies indicate that the auxin receptor and other signalling components involved in this response are sol. factors. Using an in vitro pull-down assay, we demonstrate that the interaction between transport inhibitor response 1 (TIR1) and Aux/IAA proteins does not require stable modification of either protein. Instead auxin promotes the Aux/IAA-SCFTIR1 interaction by binding directly to SCFTIR1. We further show that the loss of TIR1 and three related F-box proteins eliminates saturable auxin binding in plant exts. Finally, TIR1 synthesized in insect cells binds Aux/IAA proteins in an auxin-dependent manner. Together, these results indicate that TIR1 is an auxin receptor that mediates Aux/IAA degrdn. and auxin-regulated transcription.
- 25Dharmasiri, N.; Dharmasiri, S.; Weijers, D.; Lechner, E.; Yamada, M.; Hobbie, L.; Ehrismann, J. S.; Jürgens, G.; Estelle, M. Plant development is regulated by a family of auxin receptorF box proteins. Dev. Cell 2005, 9, 109– 119, DOI: 10.1016/j.devcel.2005.05.01424https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXmvVehurg%253D&md5=7db106eb1b509dc80d53b6a69da06a03Plant development is regulated by a family of auxin receptor F box proteinsDharmasiri, Nihal; Dharmasiri, Sunethra; Weijers, Dolf; Lechner, Esther; Yamada, Masashi; Hobbie, Lawrence; Ehrismann, Jasmin S.; Juergens, Gerd; Estelle, MarkDevelopmental Cell (2005), 9 (1), 109-119CODEN: DCEEBE; ISSN:1534-5807. (Cell Press)The plant hormone auxin has been implicated in virtually every aspect of plant growth and development. Auxin acts by promoting the degrdn. of transcriptional regulators called Aux/IAA proteins. Aux/IAA degrdn. requires TIR1, an F box protein that has been shown to function as an auxin receptor. However, loss of TIR1 has a modest effect on auxin response and plant development. Here we show that three addnl. F box proteins, called AFB1, 2, and 3, also regulate auxin response. Like TIR1, these proteins interact with the Aux/IAA proteins in an auxin-dependent manner. Plants that are deficient in all four proteins are auxin insensitive and exhibit a severe embryonic phenotype similar to the mp/arf5 and bdl/iaa12 mutants. Correspondingly, all TIR1/AFB proteins interact with BDL, and BDL is stabilized in triple mutant plants. Our results indicate that TIR1 and the AFB proteins collectively mediate auxin responses throughout plant development.
- 26Kepinski, S.; Leyser, O. The Arabidopsis TIR1 protein is an auxinreceptor. Nature 2005, 435, 446– 451, DOI: 10.1038/nature0354225https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2MXksVeisro%253D&md5=5b678dcd5c5c88a23b7d0815be915dfaThe Arabidopsis F-box protein TIR1 is an auxin receptorKepinski, Stefan; Leyser, OttolineNature (London, United Kingdom) (2005), 435 (7041), 446-451CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)Despite 100 years of evidence showing a pivotal role for indole-3-acetic acid (IAA or auxin) in plant development, the mechanism of auxin perception has remained elusive. Central to auxin response are changes in gene expression, brought about by auxin-induced interaction between the Aux/IAA transcriptional repressor proteins and the ubiquitin-ligase complex SCFTIR1, thus targeting for them proteolysis. Regulated SCF-mediated protein degrdn. is a widely occurring signal transduction mechanism. Target specificity is conferred by the F-box protein subunit of the SCF (TIR1 in the case of Aux/IAAs) and there are multiple F-box protein genes in all eukaryotic genomes examd. so far. Although SCF-target interaction is usually regulated by signal-induced modification of the target, we have previously shown that auxin signalling involves the modification of SCFTIR1. Here we show that this modification involves the direct binding of auxin to TIR1 and thus that TIR1 is an auxin receptor mediating transcriptional responses to auxin.
- 27Tan, X.; Calderon-Villalobos, L. I. A.; Sharon, M.; Zheng, C.; Robinson, C. V.; Estelle, M.; Zheng, N. Mechanism of auxinperceptionby the TIR1 ubiquitinligase. Nature 2007, 446, 640– 645, DOI: 10.1038/nature0573126https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2sXjslOlsbc%253D&md5=cbf2367ed117aeb6b1cc6e6e85f36605Mechanism of auxin perception by the TIR1 ubiquitin ligaseTan, Xu; Calderon-Villalobos, Luz Irina A.; Sharon, Michal; Zheng, Changxue; Robinson, Carol V.; Estelle, Mark; Zheng, NingNature (London, United Kingdom) (2007), 446 (7136), 640-645CODEN: NATUAS; ISSN:0028-0836. (Nature Publishing Group)Auxin is a pivotal plant hormone that controls many aspects of plant growth and development. The major naturally occurring auxin, indole-3-acetic acid (IAA), coordinates many plant growth processes by modulating gene expression, which leads to changes in cell division, elongation, and differentiation. Perceived by a small family of F-box proteins including transport inhibitor response 1 (TIR1), auxin regulates gene expression by promoting SCF ubiquitin-ligase-catalyzed degrdn. of the Aux/IAA transcription repressors, but how the TIR1 F-box protein senses and becomes activated by auxin remains unclear. Here we present the crystal structures of the Arabidopsis TIR1-ASK1 complex in ligand-free form and in complexes with three different auxin compds. and an Aux/IAA substrate peptide. These structures show that the leucine-rich repeat (LRR) domain of TIR1 contains an unexpected inositol hexakisphosphate (InsP6) co-factor and recognizes auxin and the Aux/IAA polypeptide substrate through a single surface pocket. Anchored to the base of the TIR1 pocket, auxin binds to a partially promiscuous site, which can also accommodate various auxin analogs. Docked on top of auxin, the Aux/IAA substrate peptide occupies the rest of the TIR1 pocket and completely encloses the hormone-binding site. By filling in a hydrophobic cavity at the protein interface, auxin enhances the TIR1-substrate interactions by acting as a 'mol. glue'. Our results establish the first structural model of a plant hormone receptor.
- 28European Food Safety Authority (EFSA). Draft Assessment Report Fluopyram; EFSA: Parma, Italy, Aug 15, 2011; Vol. 3, Annex B, B.7 Residue Data, pp 23– 24, http://dar.efsa.europa.eu/dar-web/provision (accessed Aug 31, 2018).There is no corresponding record for this reference.
- 29Keller, M. Phenology and Growth Cycle. In The Science of Grapevines Anatomy and Physiology, 2nd ed.; Academic Press: Cambridge, MA, 2015.There is no corresponding record for this reference.