Research progress of the resistance to succinate dehydrogenase inhibitors
-
摘要: 作用于琥珀酸脱氢酶复合体的新型杀菌剂-琥珀酸脱氢酶抑制剂 (succinate dehydrogenase inhibitors, SDHIs) 已逐步成为继Qo位点呼吸抑制剂类 (QoIs) 和麦角甾醇生物合成抑制剂类(EBIs)杀菌剂之后的世界第3大类杀菌剂。近年来，SDHIs杀菌剂的市场占有份额逐年增加，新品种不断涌现，在植物病害化学防治中发挥着重要作用。然而，由于该类杀菌剂作用位点单一，抗药性已成为制约该类杀菌剂创制发展与科学应用的重要科学问题。本综述归纳了琥珀酸脱氢酶抑制剂类杀菌剂的开发、品种、抗性发生发展、抗性分子机制与应用现状，并结合作者研究团队的最新研究成果对其靶标生物学及应用技术研究进行了总结，以期为更高活性的SDHIs杀菌剂创制和应用提供参考。Abstract: Succinate dehydrogenase inhibitors (SDHIs), targeting succinate dehydrogenase complex, have gradually become the third largest group of fungicides in the world after quinone outside inhibitors (QoIs) and ergosterol biosynthesis inhibitors (EBIs). In recent years, the market share of SDHIs is increasing yearly, and new members are emerging, playing a vital role in the chemical control of plant diseases. However, due to the single action site of these fungicides, fungicide resistance has become a key scientific issue that restricts the development and scientific application of these fungicides. In this paper, the development, products, occurrence and development of resistance, molecular mechanism and application status of SDHIs were reviewed. Together with the latest research achievements from the author's laboratory, the research on target biology and application technology was summarized, to provide references for the innovation and application of higher activity SDHIs.
-
表 1 琥珀酸脱氢酶抑制剂类杀菌剂的化学结构分类
Table 1. Classification of the chemical structure of succinate dehydrogenase inhibitors fungicides
化学结构
Chemical structure中文名称
Chinese name通用名
Common name上市时间
Announced date创制公司
Registered company呋喃-酰胺
furan-carboxamides甲呋酰胺 fenfuram 1974 壳牌和安万特 (现拜尔)
Shell and Aventis (Bayer today)N-环丙基-N-苯甲基-吡唑-酰胺
N-cyclopropyl-N-benzyl-pyrazole-carboxamides/ isoflucypram 2019 拜尔 Bayer N-甲氧基-(苯乙基)-吡唑-酰胺
N-methoxy-(phenyl-ethyl)-pyrazole-carboxamides氟唑菌酰羟胺 pydiflumetofen 2018 先正达 Syngenta 氧硫杂环己二烯-酰胺
oxathiin-carboxamides萎锈灵 carboxin 1966 尤尼罗亚尔 (现科聚亚) Uniroyal (Chemtura today) 氧化萎锈灵 oxycarboxin 1973 尤尼罗亚尔 (现科聚亚) Uniroyal (Chemtura today) 苯基-甲酰胺
phenyl-benzamides麦锈灵 benodanil 1986 巴斯夫 BASF 氟酰胺 flutolanil 1986 日本农药 Nihon Nohyaku 灭锈胺 mepronil 1981 日本组合化学
Kumiai chemical苯基-环丁基-吡啶酰胺
phenyl-cyclobutyl-pyridineamide/ cyclobutrifluram 2021 先正达 Syngenta 苯基-含氧乙基-噻吩酰胺
phenyl-oxo-ethyl-thiopheneamide异丙噻菌胺 isofetamid 2015 日本石原 Ishihara Sangyo Kaisha 吡唑-4-酰胺
pyrazole-4-carboxamides苯并烯氟菌唑 benzovindiflupyr 2012 先正达 Syngenta 联苯吡菌胺 bixafen 2011 拜耳 Bayer 氟茚唑菌胺 fluindapyr 2020 意赛格和富美实 Isagro and FMC Corporation 氟唑菌酰胺 fluxapyroxad 2011 巴斯夫 BASF 呋吡菌胺 furametpyr 1996 住友化学 Sumitomo Chemical / inpyrfluxam 2020 住友化学 Sumitomo Chemical 吡唑萘菌胺 isopyrazam 2010 先正达 Syngenta 氟唑菌苯胺 penflufen 2012 拜尔 Bayer 吡噻菌胺 penthiopyrad 2008 三井化学 Mitsui Chemicals 氟唑环菌胺 sedaxane 2011 先正达 Syngenta 吡啶-酰胺
pyridine-carboxamides啶酰菌胺 boscalid 2003 巴斯夫 BASF 吡啶基-乙基-苯甲酰胺
pyridinyl-ethyl-benzamides氟吡菌酰胺 fluopyram 2012 拜耳 Bayer 吡嗪-酰胺
pyrazine-carboxamides联苯吡嗪菌胺 pyraziflumid 2018 日本农药 Nihon Nohyaku 噻唑-酰胺
thiazole-carboxamides噻呋酰胺 thifluzamide 1997 日产化学 Nissan Chemical 苯基噻唑-酰胺
phenylthiazole-carboxamide拌种灵 amicarthiazol 1970 尤尼罗亚尔 (现科聚亚) Uniroyal (Chemtura today) 注：“ / ”代表当前该药剂尚无对应中文名。Note: "/" means that there is no corresponding Chinese name for the fungicide at present. 
下载: 导出CSV
表 2 SDHIs杀菌剂在中国的病害登记情况
Table 2. Disease registration of SDHIs fungicides in China
杀菌剂名称
Fungicide登记病害
Registered disease杀菌剂名称
Fungicide登记病害
Registered disease杀菌剂名称
Fungicide登记病害
Registered disease氟酰胺
flutolanil水稻纹枯病
Rice sheath blight异丙噻菌胺
isofetamid黄瓜灰霉病
Cucumber gray mold噻呋酰胺
thifluzamide水稻纹枯病
Rice sheath blight花生白绢病
Peanut stem rot番茄灰霉病
Tomato gray mold小麦纹枯病
Wheat sheath blight草坪褐斑病
Lawn brown spot草莓灰霉病
Strawberry gray mold花生白绢病
Peanut stem rot灭锈胺
mepronil棉花立枯病*
Cotton blight黄瓜白粉病
Cucumber powdery mildew荞麦纹枯病
Buckwheat sheath blight黄瓜立枯病*
Cucumber blight氟吡菌酰胺
fluopyram番茄根结线虫
Tomato root-knot nematode小麦锈病
Wheat rust水稻纹枯病*
Rice sheath blight香蕉根结线虫
Banana root-knot nematode马铃薯黑痣病
Potato black scurf吡噻菌胺
penthiopyrad番茄灰霉病
Tomato gray mold烟草根结线虫
Tobacco root-knot nematode茭白纹枯病
Water bamboo sheath blight葡萄灰霉病
Grape gray mold黄瓜根结线虫
Cucumber root-knot nematode水稻稻曲病
Rice false smut黄瓜白粉病
Cucumber powdery mildew黄瓜白粉病
Cucumber powdery mildew花生锈病
Peanut Rust氟唑环菌胺
sedaxane玉米丝黑穗病
Corn head smut西瓜根结线虫
Watermelon root knot nematode啶酰菌胺
boscalid马铃薯早疫病
Potato early blight玉米黑粉病
Corn smut萎锈灵
carboxin小麦锈病
Wheat Rust葡萄灰霉病
Grape gray mold氟唑菌酰羟胺
pydiflumetofen小麦赤霉病
Fusarium head blight棉花黄萎病*
Cotton verticillium wilt番茄早疫病
Tomato early blight油菜菌核病
Sclerotinia stem rot谷子黑穗病*
Millet smut黄瓜灰霉病
Cucumber gray mold草坪币斑病
Lawn leaf spot麦类黑穗病*
Wheat smut番茄灰霉病
Tomato gray mold氟唑菌苯胺
penflufen马铃薯黑痣病
Potato black scurf高粱黑穗病*
Sorghum smut草莓灰霉病
Strawberry gray mold玉米丝黑穗病
Corn head smut麦类锈病*
Wheat rust苦瓜灰霉病
Balsam pear gray mold小麦纹枯病
Wheat sheath blight玉米丝黑穗病*
Corn head smut番茄早疫病
Tomato early blight水稻恶苗病*
Rice bakanae disease氟唑菌酰胺
fluxapyroxad水稻纹枯病
Rice sheath blight油菜菌核病
Sclerotinia stem rot注：“ * ”表示曾被登记防治，现今已过登记有效期。Note: " * " indicates that it has been registered for prevention and control, and now the validity period of registration has expired.
下载: 导出CSV
表 3 植物病原菌与SDHIs杀菌剂抗性相关的点突变基因型
Table 3. Genotypes of plant pathogenic bacteria related to SDHIs fungicide resistance
报道的寄主
Hosts病害病原物
Pathogens涉及药剂
Fungicides来源
Origin突变位点
Mutation sites小麦 Wheat 亚洲镰刀菌
Fusarium asiaticum氟唑菌酰羟胺pydiflumetofen 实验室[29]
LaboratoryB-H248Y, C1a-A64V, C1a-R67K 禾谷镰刀菌
Fusarium graminearum氟唑菌酰羟胺pydiflumetofen 田间[24]
FieldC1a-A78V 立枯丝核菌
Rhizoctonia solani噻呋酰胺 thifluzamide 实验室[30]
LaboratoryB-H246Y, C-H139Y, D-H116Y 小麦壳针孢菌
Zymoseptoria tritici萎锈灵 carboxin 实验室[31-34]
LaboratoryB-N225I, B-H267Y/R/L, B-I269V, C-T79N, C-A84V,
C-N86K, C-G90R, D-H129E, C-H152R小麦壳针孢菌
Zymoseptoria triticiSDHIs 田间[23, 35-36]
FieldB-N225I, B-R265P, B-T268I/A, C-T79N/I, C-W80S,
C-N86S/A, C-R151S/T/M, C-V166M, C-T168R, D-I50F,
D-M114V, D-D129G大麦 Barley 核腔菌
Pyrenophora teresSDHIs 田间[23, 37]
FieldB-H277Y, C-N75S, C-G79R, C-H134R, C-S135R,
D-D124N/E, D-H134R, D-D145G柱隔孢菌
Ramularia collo-cygni
SDHIs田间[23]
FieldB-N224T, B-T267I, C-N87S, C-G91R, C-H146R/L,
C-H153R, C-G171D油菜 Oilseed rape 核盘菌
Sclerotinia sclerotiorum啶酰菌胺 boscalid 实验室[38]
LaboratoryB-P226L 核盘菌
Sclerotinia sclerotiorumSDHIs 田间[23]
FieldB-H273Y, C-G91R, C-H146R, C-G150R, D-T108K,
D-H132R葫芦 Gourd 泻根亚隔孢壳
Didymella bryoniae氟吡菌酰胺fluopyram 田间[39]
FieldB-H277R/Y 叉丝单囊壳白粉菌
Podosphaera xanthiiSDHIs 田间[23]
FieldB-H243Y 葫芦、黄瓜
Gourd, cucumber多主棒孢
Corynespora cassiicola啶酰菌胺 boscalid 田间[40-42]
FieldB-H278Y/R, B-I280V, C-S73P/L, C-N75S, C-H134R,
D-S89P, D-95E, D-G109V番茄、草莓、苹果
Tomato, strawberry, apple灰葡萄孢菌
Botrytis cinereaSDHIs 田间[23, 43-46]
FieldB-P225L/T/F, B-N230I, B-H272Y/R/L/V, C-G85A&I93V&M158V&V168I, C-G37S, C-I93V,
C-I79V&G85A&L151I, D-H132R花生 Peanut 米曲霉菌
Aspergillus oryzae萎锈灵 carboxin 实验室[47]
LaboratoryB-H249Y/L/N, C-T90I, D-D124E 百合 Lily 椭圆葡萄孢菌
Botrytis ellipticaSDHIs 田间[23]
FieldB-H272Y/R 玉米 Corn 玉蜀黍黑粉菌
Ustilago maydis萎锈灵 carboxin 实验室[48-49]
LaboratoryB-H257L 开心果 Pistachio 链格孢菌
Alternaria alternataSDHIs 田间[18]
FieldB-H277Y/R, C-H134R, D-D123E, D-H133R 葡萄 Grape 葡萄钩丝壳菌
Erysiphe necatorSDHIs 田间[23]
FieldB-H242R, B-I244V, C-G169D/S 芦笋 Asparagus 泡状匍柄霉菌
Stemphylium vesicariumSDHIs 田间[23]
FieldB-P225L, H272Y/R 马铃薯 Potato 茄链格孢菌，链格孢菌
A. solani, A. alternataSDHIs 田间[23]
FieldB-H278R/Y, C-H134R/Q, D-D123E, D-H133R 苹果 Apple 苹果黑星菌
Venturia inaequalisSDHIs 田间[23]
FieldB-T253I, C-H151R a：由于小麦赤霉病菌种存在两个SDHC亚基基因，以C1，C2区分。a: Due to the existence of two SDHC subunit genes in the genus of wheat scab, they are distinguished by C1 and C2.
下载: 导出CSV
-
[1] MATHRE D E. Mode of action of oxathiin systemic fungicides. I. Effect of carboxin and oxycarboxin on the general metabolism of several basidiomycetes[J]. Phytopathology, 1970, 60(4): 671-676. doi: 10.1094/Phyto-60-671 [2] AVENOT H F, MICHAILIDES T J. Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi[J]. Crop Prot, 2010, 29(7): 643-651. doi: 10.1016/j.cropro.2010.02.019 [3] SIEROTZKI H, SCALLIET G. A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides[J]. Phytopathology, 2013, 103(9): 880-887. doi: 10.1094/PHYTO-01-13-0009-RVW [4] AYER K M, VILLANI S M, CHOI M W, et al. Characterization of the VisdhC and VisdhD genes in Venturia inaequalis, and sensitivity to fluxapyroxad, pydiflumetofen, inpyrfluxam, and benzovindiflupyr[J]. Plant Dis, 2019, 103(6): 1092-1100. doi: 10.1094/PDIS-07-18-1225-RE [5] WANG J, BRADLEY C A, STENZEL O, et al. Baseline sensitivity of Fusarium virguliforme to fluopyram fungicide[J]. Plant Dis, 2017, 101(4): 576-582. doi: 10.1094/PDIS-09-16-1250-RE [6] LI W H, WU Y Q, YUAN M R, et al. Fluxapyroxad induces developmental delay in zebrafish (Danio rerio)[J]. Chemosphere, 2020, 256: 127037. doi: 10.1016/j.chemosphere.2020.127037 [7] KLITTICH C J R, WANG N X, ZHANG Y, et al. A revised model of fungicide translaminar activity[J]. Pestic Biochem Physiol, 2020, 167: 104597. doi: 10.1016/j.pestbp.2020.104597 [8] KEOHANE C E, STEELE A D, FETZER C, et al. Promysalin elicits species-selective inhibition of Pseudomonas aeruginosa by targeting succinate dehydrogenase[J]. J Am Chem Soc, 2018, 140(5): 1774-1782. doi: 10.1021/jacs.7b11212 [9] YAN Z Z, LIU A P, HUANG M Z, et al. Design, synthesis, DFT study and antifungal activity of the derivatives of pyrazolecarboxamide containing thiazole or oxazole ring[J]. Eur J Med Chem, 2018, 149: 170-181. doi: 10.1016/j.ejmech.2018.02.036 [10] YAO T T, FANG S W, LI Z S, et al. Discovery of novel succinate dehydrogenase inhibitors by the integration of in silico library design and pharmacophore mapping[J]. J Agric Food Chem, 2017, 65(15): 3204-3211. doi: 10.1021/acs.jafc.7b00249 [11] FRAC Classification of Fungicides [EB/OL]. [2022-11-01]. https://www.frac.info/docs/default-source/publications/frac-mode-of-action-poster/frac-moa-poster-2021.pdf?sfvrsn=a6f6499a_2. [12] LI H, GAO M Q, CHEN Y, et al. Discovery of pyrazine-carboxamide-diphenyl-ethers as novel succinate dehydrogenase inhibitors via fragment recombination[J]. J Agric Food Chem, 2020, 68(47): 14001-14008. doi: 10.1021/acs.jafc.0c05646 [13] GAO Y Y, HE L F, ZHU J M, et al. The relationship between features enabling SDHI fungicide binding to the Sc-Sdh complex and its inhibitory activity against Sclerotinia sclerotiorum[J]. Pest Manag Sci, 2020, 76(8): 2799-2808. doi: 10.1002/ps.5827 [14] 中国农药信息网 [EB/OL]. [2022-11-01]. http://www.chinapesticide.org.cn/. [15] DOOLEY H, SHAW M W, SPINK J, et al. The effect of succinate dehydrogenase inhibitor/azole mixtures on selection of Zymoseptoria tritici isolates with reduced sensitivity[J]. Pest Manag Sci, 2016, 72(6): 1150-1159. doi: 10.1002/ps.4093 [16] GUNATILLEKE I A, ARST H N, Jr, SCAZZOCCHIO C. Three genes determine the carboxin sensitivity of mitochondrial succinate oxidation in Aspergillus nidulans[J]. Genet Res, 1975, 26(3): 297-305. doi: 10.1017/S0016672300016098 [17] LUCAS J A, HAWKINS N J, FRAAIJE B A. The evolution of fungicide resistance[J]. Adv Appl Microbiol, 2015, 90(29): 29-92. [18] AVENOT H F, SELLAM A, KARAOGLANIDIS G, et al. Characterization of mutations in the iron-sulphur subunit of succinate dehydrogenase correlating with boscalid resistance in Alternaria alternata from California pistachio[J]. Phytopathology, 2008, 98(6): 736-742. doi: 10.1094/PHYTO-98-6-0736 [19] STRAYER SCHERER A L, REEVES E, HENSON M, et al. Prevalence of mutations conferring resistance to QoI and SDHI fungicides in the early blight pathogens on tomato (Alternaria spp.)[J]. Phytopathology, 2021, 111(S10): 5. [20] MILES T D, FAIRCHILD K L, MERLINGTON A, et al. First report of boscalid and penthiopyrad-resistant isolates of Alternaria solani causing early blight of potato in Michigan[J]. Plant Dis, 2013, 97(12): 1655-1656. [21] VICENTINI S N C, CASADO P S, CARVALHO G, et al. Monitoring of Brazilian wheat blast field populations reveals resistance to QoI, DMI, and SDHI fungicides[J]. Plant Pathol, 2022, 71(2): 304-321. doi: 10.1111/ppa.13470 [22] MATSUZAKI Y, HARADA T, IWAHASHI F. Amino acid substitutions responsible for different QoI and SDHI sensitivity patterns in Puccinia horiana, the causal agent of chrysanthemum white rust[J]. Plant Pathol, 2021, 70(2): 377-386. doi: 10.1111/ppa.13298 [23] Monitoring Results and Use Recommendations [EB/OL]. [2022-11-01]. https://www.frac.info/frac-teams/working-groups/sdhi-fungicides/recommendations-for-sdhi. [24] SHAO W Y, WANG J R, WANG H Y, et al. Fusarium graminearum FgSdhC1 point mutation A78V confers resistance to the succinate dehydrogenase inhibitor pydiflumetofen[J]. Pest Manag Sci, 2022, 78(5): 1780-1788. doi: 10.1002/ps.6795 [25] LIU S M, FU L Y, TAN H H, et al. Resistance to boscalid in Botrytis cinerea from greenhouse-grown tomato[J]. Plant Dis, 2021, 105(3): 628-635. doi: 10.1094/PDIS-06-20-1191-RE [26] FAN Z, YANG J H, FAN F, et al. Fitness and competitive ability of Alternaria alternata field isolates with resistance to SDHI, QoI, and MBC fungicides[J]. Plant Dis, 2015, 99(12): 1744-1750. doi: 10.1094/PDIS-03-15-0354-RE [27] DUAN Y B, XIN W J, LU F, et al. Benzimidazole- and QoI-resistance in Corynespora cassiicola populations from greenhouse-cultivated cucumber: an emerging problem in China[J]. Pestic Biochem Physiol, 2019, 153: 95-105. doi: 10.1016/j.pestbp.2018.11.006 [28] MAIR W, LOPEZ-RUIZ F, STAMMLER G, et al. Proposal for a unified nomenclature for target-site mutations associated with resistance to fungicides[J]. Pest Manag Sci, 2016, 72(8): 1449-1459. doi: 10.1002/ps.4301 [29] CHEN W C, WEI L L, ZHAO W C, et al. Resistance risk assessment for a novel succinate dehydrogenase inhibitor pydiflumetofen in Fusarium asiaticum[J]. Pest Manag Sci, 2021, 77(1): 538-547. doi: 10.1002/ps.6053 [30] SUN H Y, LU C Q, LI W, et al. Homozygous and heterozygous point mutations in succinate dehydrogenase subunits b, c and d of Rhizoctonia cerealis conferring resistance to thifluzamide[J]. Pest Manag Sci, 2017, 73(5): 896-903. doi: 10.1002/ps.4361 [31] SCALLIET G, BOWLER J, LUKSCH T, et al. Mutagenesis and functional studies with succinate dehydrogenase inhibitors in the wheat pathogen Mycosphaerella graminicola[J]. PLoS One, 2012, 7(4): e35429. doi: 10.1371/journal.pone.0035429 [32] FRAAIJE B A, BAYON C, ATKINS S, et al. Risk assessment studies on succinate dehydrogenase inhibitors, the new weapons in the battle to control Septoria leaf blotch in wheat[J]. Mol Plant Pathol, 2012, 13(3): 263-275. doi: 10.1111/j.1364-3703.2011.00746.x [33] GUTIÉRREZ-ALONSO O, HAWKINS N J, COOLS H J, et al. Dose-dependent selection drives lineage replacement during the experimental evolution of SDHI fungicide resistance in Zymoseptoria tritici[J]. Evol Appl, 2017, 10(10): 1055-1066. doi: 10.1111/eva.12511 [34] SKINNER W, BAILEY A, RENWICK A, et al. A single amino-acid substitution in the iron-sulphur protein subunit of succinate dehydrogenase determines resistance to carboxin in Mycosphaerella graminicola[J]. Curr Genet, 1998, 34(5): 393-398. doi: 10.1007/s002940050412 [35] HELLIN P, DUVIVIER M, HEICK T M, et al. Spatio-temporal distribution of DMI and SDHI fungicide resistance of Zymoseptoria tritici throughout Europe based on frequencies of key target-site Alterations[J]. Pest Manag Sci, 2021, 77(12): 5576-5588. doi: 10.1002/ps.6601 [36] REHFUS A, STROBEL D, BRYSON R, et al. Mutations in sdh genes in field isolates of Zymoseptoria tritici and impact on the sensitivity to various succinate dehydrogenase inhibitors[J]. Plant Pathol, 2018, 67(1): 175-180. doi: 10.1111/ppa.12715 [37] REHFUS A, MIESSNER S, ACHENBACH J, et al. Emergence of succinate dehydrogenase inhibitor resistance of Pyrenophora teres in Europe[J]. Pest Manag Sci, 2016, 72(10): 1977-1988. doi: 10.1002/ps.4244 [38] WANG Q, MAO Y S, LI S X, et al. Molecular mechanism of Sclerotinia sclerotiorum resistance to succinate dehydrogenase inhibitor fungicides[J]. J Agric Food Chem, 2022, 70(23): 7039-7048. doi: 10.1021/acs.jafc.2c02056 [39] AVENOT H F, THOMAS A, GITAITIS R D, et al. Molecular characterization of boscalid- and penthiopyrad-resistant isolates of Didymella bryoniae and assessment of their sensitivity to fluopyram[J]. Pest Manag Sci, 2012, 68(4): 645-651. doi: 10.1002/ps.2311 [40] MIYAMOTO T, ISHII H, STAMMLER G, et al. Distribution and molecular characterization of Corynespora cassiicola isolates resistant to boscalid[J]. Plant Pathol, 2010, 59(5): 873-881. doi: 10.1111/j.1365-3059.2010.02321.x [41] ZHU F D, SHI Y X, XIE X W, et al. Occurrence, distribution, and characteristics of boscalid-resistant Corynespora cassiicola in China[J]. Plant Dis, 2019, 103(1): 69-76. doi: 10.1094/PDIS-11-17-1760-RE [42] MIYAMOTO T, ISHII H, SEKO T, et al. Occurrence of Corynespora cassiicola isolates resistant to boscalid on cucumber in Ibaraki Prefecture, Japan[J]. Plant Pathol, 2009, 58(6): 1144-1151. doi: 10.1111/j.1365-3059.2009.02151.x [43] YIN Y N, KIM Y K, XIAO C L. Molecular characterization of boscalid resistance in field isolates of Botrytis cinerea from apple[J]. Phytopathology, 2011, 101(8): 986-995. doi: 10.1094/PHYTO-01-11-0016 [44] VELOUKAS T, LEROCH M, HAHN M, et al. Detection and molecular characterization of boscalid-resistant Botrytis cinerea isolates from strawberry[J]. Plant Dis, 2011, 95(10): 1302-1307. doi: 10.1094/PDIS-04-11-0317 [45] De MICCOLIS ANGELINI R M, HABIB W, ROTOLO C, et al. Selection, characterization and genetic analysis of laboratory mutants of Botryotinia fuckeliana (Botrytis cinerea) resistant to the fungicide boscalid[J]. Eur J Plant Pathol, 2010, 128(2): 185-199. doi: 10.1007/s10658-010-9643-8 [46] BARDAS G A, VELOUKAS T, KOUTITA O, et al. Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups[J]. Pest Manag Sci, 2010, 66(9): 967-973. doi: 10.1002/ps.1968 [47] SHIMA Y, ITO Y, KANEKO S, et al. Identification of three mutant loci conferring carboxin-resistance and development of a novel transformation system in Aspergillus oryzae[J]. Fungal Genet Biol, 2009, 46(1): 67-76. doi: 10.1016/j.fgb.2008.10.005 [48] BROOMFIELD P L E, HARGREAVES J A. A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis[J]. Curr Genet, 1992, 22(2): 117-121. doi: 10.1007/BF00351470 [49] KEON J P R, WHITE G A, HARGREAVES J A. Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis[J]. Curr Genet, 1991, 19(6): 475-481. doi: 10.1007/BF00312739 [50] BAUSKE M J, YELLAREDDYGARI S K R, GUDMESTAD N C. Potential impact of fluopyram on the frequency of the D123E mutation in Alternaria solani[J]. Plant Dis, 2018, 102(3): 656-665. doi: 10.1094/PDIS-06-17-0853-RE [51] LANDSCHOOT S, CARRETTE J, VANDECASTEELE M, et al. Boscalid-resistance in Alternaria alternata and Alternaria solani populations: an emerging problem in Europe[J]. Crop Prot, 2017, 92: 49-59. doi: 10.1016/j.cropro.2016.10.011 [52] SHAO W Y, ZHAO Y F, MA Z H. Advances in understanding fungicide resistance in Botrytis cinerea in China[J]. Phytopathology, 2021, 111(3): 455-463. doi: 10.1094/PHYTO-07-20-0313-IA [53] LI H X, NUCKOLS T A, HARRIS D, et al. Differences in fungicide resistance profiles and multiple resistance to a quinone-outside inhibitor (QoI), two succinate dehydrogenase inhibitors (SDHI), and a demethylation inhibitor (DMI) for two Stagonosporopsis species causing gummy stem blight of cucurbits[J]. Pest Manag Sci, 2019, 75(11): 3093-3101. doi: 10.1002/ps.5426 [54] HU M J, FERNÁNDEZ-ORTUÑO D, SCHNABEL G. Monitoring resistance to SDHI fungicides in Botrytis cinerea from strawberry fields[J]. Plant Dis, 2016, 100(5): 959-965. doi: 10.1094/PDIS-10-15-1210-RE [55] FERNÁNDEZ-ORTUÑO D, PÉREZ-GARCÍA A, CHAMORRO M, et al. Resistance to the SDHI fungicides boscalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from commercial strawberry fields in Spain[J]. Plant Dis, 2017, 101(7): 1306-1313. doi: 10.1094/PDIS-01-17-0067-RE [56] HAWKINS N J, FRAAIJE B A. Fitness penalties in the evolution of fungicide resistance[J]. Annu Rev Phytopathol, 2018, 56: 339-360. doi: 10.1146/annurev-phyto-080417-050012 [57] AMIRI A, ZUNIGA A I, PERES N A. Mutations in the membrane-anchored SdhC subunit affect fitness and sensitivity to succinate dehydrogenase inhibitors in Botrytis cinerea populations from multiple hosts[J]. Phytopathology, 2020, 110(2): 327-335. doi: 10.1094/PHYTO-07-19-0240-R [58] YAMASHITA M, FRAAIJE B. Non-target site SDHI resistance is present as standing genetic variation in field populations of Zymoseptoria tritici[J]. Pest Manag Sci, 2018, 74(3): 672-681. doi: 10.1002/ps.4761 [59] MÄE A, FILLINGER S, SOOVÄLI P, et al. Fungicide sensitivity shifting of Zymoseptoria tritici in the finnish-baltic region and a novel insertion in the MFS1 promoter[J]. Front Plant Sci, 2020, 11: 385. doi: 10.3389/fpls.2020.00385 [60] SANG H, CHANG H X, CHOI S, et al. Genome-wide transcriptional response of the causal soybean sudden death syndrome pathogen Fusarium virguliforme to a succinate dehydrogenase inhibitor fluopyram[J]. Pest Manag Sci, 2022, 78(2): 530-540. doi: 10.1002/ps.6657 [61] 张晓柯, 韩絮, 马薇薇, 等. 江苏省草莓灰霉病菌对氟吡菌酰胺敏感性基线的建立及抗性风险评估[J]. 南京农业大学学报, 2015, 38(5): 810-815. doi: 10.7685/j.issn.1000-2030.2015.05.016ZHANG X K, HAN X, MA W W, et al. Baseline sensitivity of fluopyram and its resistance risk assessment against Botrytis cinerea from strawberry in Jiangsu Province[J]. J Nanjing Agric Univ, 2015, 38(5): 810-815. doi: 10.7685/j.issn.1000-2030.2015.05.016 [62] ISHII H, MIYAMOTO T, USHIO S, et al. Lack of cross-resistance to a novel succinate dehydrogenase inhibitor, fluopyram, in highly boscalid-resistant isolates of Corynespora cassiicola and Podosphaera xanthii[J]. Pest Manag Sci, 2011, 67(4): 474-482. doi: 10.1002/ps.2092 [63] STEINHAUER D, SALAT M, FREY R, et al. A dispensable paralog of succinate dehydrogenase subunit C mediates standing resistance towards a subclass of SDHI fungicides in Zymoseptoria tritici[J]. PLoS Pathog, 2019, 15(12): e1007780. doi: 10.1371/journal.ppat.1007780 [64] SHAO W Y, SUN J T, ZHANG X K, et al. Amino acid polymorphism in succinate dehydrogenase subunit C involved in biological fitness of Botrytis cinerea[J]. Mol Plant Microbe Interact, 2020, 33(4): 580-589. doi: 10.1094/MPMI-07-19-0187-R [65] 毛玉帅. 油菜菌核病菌 (Sclerotinia sclerotiorum) 抗药性监测及治理技术研发[D]. 南京: 南京农业大学, 2020.MAO Y S. Research and development of drug resistance monitoring and control technology of Sclerotinia sclerotiorum[D]. Nanjing: Nanjing Agricultural University, 2020. [66] 李美霞. 小麦赤霉病菌呼吸链系统关键基因对呼吸链抑制剂类杀菌剂药敏性的调控作用研究[D]. 南京: 南京农业大学, 2019.LI M X. Regulation effect of key genes in respiratory chain system on sensitivity of Fusarium asiaticum to respiratory inhibitor fungicides[D]. Nanjing: Nanjing Agricultural University, 2019. [67] 仇剑波. 禾谷镰孢菌 β-微管蛋白基因定点突变及敲除对多菌灵敏感性和基因表达谱的影响[D]. 南京: 南京农业大学, 2012.QIU J B. Effect of site-directed mutagenesis and gene deletion of Gibberella Zeae β-tubulin on its sensitivity to carbendazim and gene expression proflie[D]. Nanjing: Nanjing Agricultural University, 2012. [68] YANG J H, BRANNEN P M, SCHNABEL G. Resistance in Alternaria alternata to SDHI fungicides causes rare disease outbreak in peach orchards[J]. Plant Dis, 2015, 99(1): 65-70. doi: 10.1094/PDIS-04-14-0387-RE [69] GUDMESTAD N C, ARABIAT S, MILLER J S, et al. Prevalence and impact of SDHI fungicide resistance in Alternaria solani[J]. Plant Dis, 2013, 97(7): 952-960. doi: 10.1094/PDIS-12-12-1176-RE [70] AVENOT H, SELLAM A, MICHAILIDES T. Characterization of mutations in the membrane-anchored subunits AaSDHC and AaSDHD of succinate dehydrogenase from Alternaria alternata isolates conferring field resistance to the fungicide boscalid[J]. Plant Pathol, 2009, 58(6): 1134-1143. doi: 10.1111/j.1365-3059.2009.02154.x [71] LEE J, ELLIOTT M R, KIM M, et al. A rapid molecular detection system for SdhB and SdhC point mutations conferring differential succinate dehydrogenase inhibitor resistance in Clarireedia populations[J]. Plant Dis, 2021, 105(3): 660-666. doi: 10.1094/PDIS-04-20-0724-RE [72] CHATZIDIMOPOULOS M, GANOPOULOS I, MADESIS P, et al. High-resolution melting analysis for rapid detection and characterization of Botrytis cinerea phenotypes resistant to fenhexamid and boscalid[J]. Plant Pathol, 2014, 63(6): 1336-1343. doi: 10.1111/ppa.12210 [73] LICHTEMBERG P S F, LUO Y, DOUSSOULIN H, et al. Using Allele-specific PCR for detecting multiple amino acid substitutions associated with SDHI resistance in Alternaria alternata causing Alternaria late blight in pistachio[J]. Lett Appl Microbiol, 2018, 67(5): 506-512. doi: 10.1111/lam.13064 [74] DUAN Y B, GE C Y, ZHANG X K, et al. A rapid detection method for the plant pathogen Sclerotinia sclerotiorum based on loop-mediated isothermal amplification (LAMP)[J]. Australasian Plant Pathol, 2014, 43(1): 61-66. doi: 10.1007/s13313-013-0239-6 [75] DUAN Y B, YANG Y, WANG J X, et al. Development and application of loop-mediated isothermal amplification for detecting the highly benzimidazole-resistant isolates in Sclerotinia sclerotiorum[J]. Sci Rep, 2015, 5: 17278. doi: 10.1038/srep17278 [76] DUAN Y B, YANG Y, WANG Y, et al. Loop-mediated isothermal amplification for the rapid detection of the F200Y mutant genotype of carbendazim-resistant isolates of Sclerotinia sclerotiorum[J]. Plant Dis, 2016, 100(5): 976-983. doi: 10.1094/PDIS-10-15-1185-RE [77] DUAN Y B, YANG Y, LI T, et al. Development of a rapid and high-throughput molecular method for detecting the F200Y mutant genotype in benzimidazole-resistant isolates of Fusarium asiaticum[J]. Pest Manag Sci, 2016, 72(11): 2128-2135. doi: 10.1002/ps.4243 [78] DUAN Y B, YANG Y, WANG J X, et al. Simultaneous detection of multiple benzimidazole-resistant β-tubulin variants of Botrytis cinerea using loop-mediated isothermal amplification[J]. Plant Dis, 2018, 102(10): 2016-2024. doi: 10.1094/PDIS-03-18-0542-RE [79] ZHU J M, ZHANG L Y, LI H, et al. Development of a LAMP method for detecting the N75S mutant in SDHI-resistant Corynespora cassiicola[J]. Anal Biochem, 2020, 597: 113687. doi: 10.1016/j.ab.2020.113687 [80] FAN F, YIN W X, LI G Q, et al. Development of a LAMP method for detecting SDHI fungicide resistance in Botrytis cinerea[J]. Plant Dis, 2018, 102(8): 1612-1618. doi: 10.1094/PDIS-12-17-1933-RE [81] 段亚冰, 周明国, 陈长军, 等. 一种快速检测灰葡萄孢菌对 SDHI 类杀菌剂抗性的方法及引物组合物: CN105063187A[P]. 2015-11-18.DUAN Y B, ZHOU M G, CHEN C J, et al. Method and primer composition for rapid detection of resistance of Botrytis cinerea to SDH1 fungicides: CN105063187A[P]. 2015-11-18. [82] AMIRI A, HEATH S M, PERES N A. Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry[J]. Plant Dis, 2014, 98(4): 532-539. doi: 10.1094/PDIS-07-13-0753-RE [83] SAMARAS A, HADJIPETROU C, KARAOGLANIDIS G. Bacillus amyloliquefaciens strain QST713 may contribute to the management of SDHI resistance in Botrytis cinerea[J]. Pest Manag Sci, 2021, 77(3): 1316-1327. doi: 10.1002/ps.6145 [84] VAN DEN BOSCH F, PAVELEY N, VAN DEN BERG F, et al. Mixtures as a fungicide resistance management tactic[J]. Phytopathology, 2014, 104(12): 1264-1273. doi: 10.1094/PHYTO-04-14-0121-RVW [85] ZHANG L, LI W, XIAO T F, et al. Design and discovery of novel chiral antifungal amides with 2-(2-oxazolinyl) aniline as a promising pharmacophore[J]. J Agric Food Chem, 2018, 66(34): 8957-8965. doi: 10.1021/acs.jafc.8b02778 -
