Recent Advances in Molecular Mechanisms of Plant Responses Against Botrytis cinerea

doi:10.13560/j.cnki.biotech.bull.1985.2018-0040

Abstract

Abstract: Botrytis cinerea,the gray mold fungus,is a broad host-range necrotrophic agent. This necrotrophic fungus adopts diverse virulence strategies to aggress host plants. And correspondingly,defense responses of host plants are multifaceted and genetically quantitative. PTI is the important part of immune responses to B. cinerea. In this review,recent advances in signals eliciting PTI and recognition,transmission of B. cinerea signals,transcriptional factors and epigenetic modifications,plant hormone regulation,resistant cellular events and secondary metabolites are summarized. Elements and methods for applying in gray mold management practices are particularly pointed out,for the purpose of resolving problems resulted from using chemical pesticides only.

Key words: defense responses, molecular mechanisms, the gray mold fungus B. cinerea

ZHANG Yan, XIA Geng-shou, LAI Zhi-bing. Recent Advances in Molecular Mechanisms of Plant Responses Against Botrytis cinerea[J]. Biotechnology Bulletin, 2018, 34(2): 10-24.

References

[1] Williamson B, Tudzynski B, Tudzynski P, et al.Botrytis cinerea:the cause of grey mould disease[J]. Molecular Plant Pathology, 2007, 8:561-580.
[2] Elad Y, Pertot I, Cotes Prado AM, Stewart A.Plant hosts of Botrytis spp[M]//Fillinger S, Elad Y, eds. Botrytis-the fungus, the pathogen and its management in agricultural systems. Heidelberg.Germany:Springer, 2016:413-486.
[3] Dean R, Van Kan JA, Pretorius ZA, et al.The top 10 fungal pathogens in molecular plant pathology[J]. Molecular Plant Pathology, 2012, 13:414-430.
[4] Veloukas T, Kalogeropoulou P, Markoglou AN, et al.Fitness and competitive ability of Botrytis cinerea field isolates with dual resistance to SDHI and QoI fungicides, associated with several sdhB and the cytb G143A mutations[J]. Phytopathology, 2014, 104:347-356.
[5] Rupp S, Plesken C, Rumsey S, et al. Botrytis fragariae, a new species causing gray mold on strawberries, shows high frequencies of specific and efflux-based fungicide resistance[J]. Applied and Environmental Microbiology, 2017, 83(9). pii:e00269-17.
[6] Lai Z, Mengiste T.Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens[J]. Current Opinion in Plant Biology, 2013, 16:505-512.
[7] Mengiste T.Plant immunity to necrotrophs[J]. Annual Review of Phytopathology, 2012, 50:267-294.
[8] Liu T, Liu Z, Song C, et al.Chitin-induced dimerization activates a plant immune receptor[J]. Science, 2012, 336:1160-1164.
[9] Núñez de Cáceres González FF, Davey MR, Cancho Sanchez E, et al. Conferred resistance to Botrytis cinerea in Lilium by overexpression of the RCH10 chitinase gene[J]. Plant Cell Reports, 2015, 34:1201-1209.
[10] Gao Y, Jia S, Wang C, et al.BjMYB1, a transcription factor implicated in plant defence through activating BjCHI1 chitinase expression by binding to a W-box-like element[J]. Journal of Experimental Botany, 2016, 67:4647-4658.
[11] Gao Y, Zhao K.Molecular mechanism of BjCHI1-mediated plant defense against Botrytis cinerea infection[J]. Plant Signaling & Behavior, 2017, 12:e1271859.
[12] Gai YP, Zhao YN, Zhao HN, et al.The latex protein MLX56 from mulberry(Morus multicaulis)protects plants against insect pests and pathogens[J]. Frontiers in Plant Science, 2017, 8:1475.
[13] Prins T, Tudzynski P, Tiedemann A, et al.Infection strategies of Botrytis cinerea and related necrotrophic pathogens. In Fungal Pathology[M]// JW Kronstad Dordrecht. The Netherlands:Kluwer, 2000:33-64.
[14] Rasul S, Dubreuil-Maurizi C, Lamotte O, et al.Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana[J]. Plant, Cell & Environment, 2012, 35:1483-1499.
[15] Davidsson P, Broberg M, Kariola T, et al.Short oligogalacturonides induce pathogen resistance-associated gene expression in Arabidopsis thaliana[J]. BMC Plant Biology, 2017, 17:19.
[16] Lionetti V, Raiola A, Camardella L, et al.Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea[J]. Plant Physiology, 2007, 143:1871-1880.
[17] Reem NT, Pogorelko G, Lionetti V, et al.Decreased polysaccharide feruloylation compromises plant cell wall integrity and increases susceptibility to necrotrophic fungal pathogens[J]. Frontiers in Plant Science, 2016, 7:630.
[18] Fauth M, Schweizer P, Buchala A, et al.Cutin monomers and surface wax constituents elicit H₂O₂ in conditioned cucumber hypocotyl segments and enhance the activity of other H₂O₂ elicitors[J]. Plant Physiology, 1998, 117:1373-1380.
[19] Schweizer P, Felix G, Buchala A, et al.Perception of free cutin monomers by plant cells[J]. The Plant Journal, 1996, 10:331-341.
[20] Voisin D, Nawrath C, Kurdyukov S, et al.Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator[J]. PLoS Genetics, 2015, 5(10):e1000703.
[21] L’Haridon F, Besson-Bard A, Binda M, et al. A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity[J]. PLoS Pathogens, 2011, 7(7):e1002148.
[22] Bessire M, Chassot C, Jacquat AC, et al.A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea[J]. The EMBO Journal, 2007, 26:2158-2168.
[23] Ju S, Go YS, Choi HJ, et al.DEWAX transcription factor is involved in resistance to Botrytis cinerea in Arabidopsis thaliana and Camelina sativa[J]. Frontiers in Plant Science, 2017, 8:1210.
[24] Go YS, Kim H, Kim HJ, et al.Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-Type transcription factor[J]. The Plant Cell, 2014, 26:1666-1680.
[25] Zhang H, Yu P, Zhao J, et al.Expression of tomato prosystemin gene in Arabidopsis reveals systemic translocation of its mRNA and confers necrotrophic fungal resistance[J]. The New Phytologist, 2017, 217:799-812.
[26] Liu Z, Wu Y, Yang F, et al.BIK1 interacts with PEPRs to mediate ethylene-induced immunity[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110:6205-6210.
[27] Ross A, Yamada K, Hiruma K, et al.The Arabidopsis PEPR pathway couples local and systemic plant immunity[J]. The EMBO Journal, 2014, 33:62-75.
[28] Tang D, Zhou JM.PEPRs spice up plant immunity[J]. The EMBO Journal, 2016, 35:4-5.
[29] Yamada K, Yamashita-Yamada M, Hirase T, et al.Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1[J]. The EMBO Journal, 2016, 35:46-61.
[30] Miya A, Albert P, Shinya T, et al.CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104:19613-19618.
[31] Chinchilla D, Zipfel C, Robatzek S, et al.A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence[J]. Nature, 2007, 448:497-500.
[32] Kemmerling B, Schwedt A, Rodriguez P, et al.The BRI1-associated kinase 1, BAK1, has a brassinolide-Independent role in plant cell-death control[J]. Current Biology, 2007, 17:1116-1122.
[33] Schulze B, Mentzel T, Jehle AK, et al.Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1[J]. The Journal of Biological Chemistry, 2010, 285:9444-9451.
[34] Veronese P, Nakagami H, Bluhm B, et al.The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens[J]. The Plant Cell, 2006, 18:257-273.
[35] Laluk K, Luo H, Chai M, et al.Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis[J]. The Plant Cell, 2011, 23:2831-2849.
[36] Zhang J, Li W, Xiang T, et al.Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector[J]. Cell Host & Microbe, 2010, 7:290-301.
[37] Feng F, Yang F, Rong W, et al.A Xanthomonas uridine 5’-monop-hosphate transferase inhibits plant immune kinases[J]. Nature, 2012, 485:114-118.
[38] Galletti R, Ferrari S, De Lorenzo G.Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea[J]. Plant Physiology, 2011, 157:804-814.
[39] Genenncher B, Wirthmueller L, Roth C, et al.Nucleoporin-regulated MAP kinase signaling in immunity to a necrotrophic fungal pathogen[J]. Plant Physiology, 2016, 172:1293-1305.
[40] Meng X, Xu J, He Y, et al.Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance[J]. The Plant Cell, 2013, 25:1126-1142.
[41] Jiang Y, Yu D.The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise Botrytis cinerea resistance[J]. Plant Physiology, 2016, 171:2771-2782.
[42] Birkenbihl RP, Diezel C, Somssich IE.Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection[J]. Plant Physiology, 2012, 159:266-285.
[43] Lai Z, Vinod K, Zheng Z, et al.Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens[J]. BMC Plant Biology, 2008, 8:68.
[44] Liu S, Kracher B, Ziegler J, et al.Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100[J]. ELife, 2015, 4:e07295.
[45] Li GJ, Meng XZ, Wang RG, et al.Dual-Level Regulation of ACC Synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis[J]. PLoS Genetics, 2012, 8(6):e1002767.
[46] Liao CJ, Lai ZB, Lee S, et al.Arabidopsis HOOKLESS1 regulates responses to pathogens and abscisic acid through interaction with MED18 and acetylation of WRKY33 and ABI5 chromatin[J]. The Plant Cell, 2016, 28:1662-1681.
[47] Liu B, Hong YB, Zhang YF, et al.Tomato WRKY transcriptional factor SlDRW1 is required for disease resistance against Botrytis cinerea and tolerance to oxidative stress[J]. Plant Science:an International Journal of Experimental Plant Biology, 2014, 227:145-156.
[48] Adachi H, Ishihama N, Nakano T, et al.Nicotiana benthamiana MAPK-WRKY pathway confers resistance to a necrotrophic pathogen Botrytis cinerea[J]. Plant Signaling & Behavior, 2016, 11:e1183085.
[49] Zhao Y, Wei T, Yin KQ, et al.Arabidopsis RAP2. 2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses[J]. The New Phytologist, 2012, 195:450-460.
[50] Moffat CS, Ingle RA, Wathugala DL, et al.ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis[J]. PLoS One, 2012, 7(4):e3599.
[51] Zhang H, Hong Y, Huang L, et al.Arabidopsis AtERF014 acts as a dual regulator that differentially modulates immunity against Pseudomonas syringae pv. tomato and Botrytis cinerea[J]. Scientific Reports, 2016, 6:30251.
[52] Lu X, Jiang W, Zhang L, et al.AaERF1 positively regulates the resistance to Botrytis cinerea in Artemisia annua[J]. PLoS One, 2013, 8:e57657.
[53] Lu X, Zhang L, Zhang F, et al.AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea[J]. The New Phytologist, 2013, 198:1191-1202.
[54] Ramirez V, Agorio A, Coego A, et al.MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis[J]. Plant Physiology, 2011, 155:1920-1935.
[55] Sardesai N, Laluk K, Mengiste T, et al. The Arabidopsis Myb transcription factor MTF1 is a unidirectional regulator of susceptibility to Agrobacterium[J]. Plant Signaling & Behavior, 2014, 9. pii:e28983.
[56] Krol E, Mentzel T, Chinchilla D, et al.Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2[J]. The Journal of Biological Chemistry, 2010, 285:13471-13479.
[57] Giri MK, Singh N, Banday ZZ, et al.GBF1 differentially regulates CAT2 and PAD4 transcription to promote pathogen defense in Arabidopsis thaliana[J]. The Plant Journal:for Cell and Molecular Biology, 2017, 91:802-815.
[58] Yang Y, Li L, Qu LJ.Plant Mediator complex and its critical functions in transcription regulation[J]. Journal of Integrative Plant Biology, 2016, 58:106-118.
[59] Kidd BN, Edgar CI, Kumar KK, et al.The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis[J]. The Plant Cell, 2009, 21:2237-2252.
[60] Cevik V, Kidd BN, Zhang P, et al.MEDIATOR25 acts as an integra-
tive hub for the regulation of jasmonate-responsive gene expression in Arabidopsis[J]. Plant Physiology, 2012, 160:541-555.
[61] Ou B, Yin KQ, Liu SN, et al.A high-throughput screening system for Arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation[J]. Molecular Plant, 2011, 4:546-555.
[62] Yang Y, Ou B, Zhang J, et al.The Arabidopsis Mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25[J]. The Plant Journal:for Cell and Molecular Biology, 2014, 77:838-851.
[63] Chen R, Jiang H, Li L, et al.The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors[J]. The Plant Cell, 2012, 24:2898-2916.
[64] Lai Z, Schluttenhofer CM, Bhide K, et al.MED18 interaction with distinct transcription factors regulates multiple plant functions[J]. Nature Communications, 2014, 5:3064.
[65] Zhu Y, Schluttenhoffer CM, Wang P, et al.CYCLIN-DEPENDENT KINASE8 differentially regulates plant immunity to fungal pathogens through kinase-dependent and -independent functions in Arabidopsis[J]. The Plant Cell, 2014, 26:4149-4170.
[66] Wang C, Du X, Mou Z.The mediator complex subunits MED14, MED15, and MED16 are involved in defense signaling crosstalk in Arabidopsis[J]. Frontiers in Plant Science, 2016, 7:1947.
[67] Wang C, Ding Y, Yao J, Zhang Y, et al.Arabidopsis Elongator subunit 2 positively contributes to resistance to the necrotrophic fungal pathogens Botrytis cinerea and Alternaria brassicicola[J]. The Plant Journal, 2015, 83:1019-1033.
[68] Wang C, Zhang X, Li JL, Zhang Y, et al.The Elongator complex-associated protein DRL1 plays a positive role in immune responses against necrotrophic fungal pathogens in Arabidopsis[J]. Molecular Plant Pathology, 2016, 19:286-299.
[69] Berr A, McCallum EJ, Alioua A, et al. Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi[J]. Plant Physiology, 2010, 154:1403-1414.
[70] Lee S, Fu F, Xu S, et al.Global regulation of plant immunity by histone lysine methyl transferases[J]. The Plant Cell, 2016, 28:1640-1661.
[71] Lopez A, Ramirez V, Garcia-Andrade J, et al.The RNA silencing enzyme RNA polymerase v is required for plant immunity[J]. PLoS Genetics, 2011, 7:e1002434.
[72] Dhawan R, Luo H, Foerster AM, et al.HISTONE MONOUBIQUI-TINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis[J]. The Plant Cell, 2009, 21:1000-1019.
[73] Zhang Y, Li D, Zhang H, et al.Tomato histone H2B monoubiquitination enzymes SlHUB1 and SlHUB2 contribute to disease resistance against Botrytis cinerea through modulating the balance between SA- and JA/ET-mediated signaling pathways[J]. BMC Plant Biology, 2015, 15:252.
[74] El Oirdi M, El Rahman TA, Rigano L, et al.Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato[J]. The Plant Cell, 2011, 23:2405-2421.
[75] Asselbergh B, Curvers K, Franca SC, et al.Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis[J]. Plant Physiology, 2007, 144:1863-1877.
[76] Abuqamar S, Luo H, Laluk K, et al.Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor[J]. The Plant Journal:for Cell and Molecular Biology, 2009, 58:347-360.
[77] Ouyang Z, Liu S, Huang L, et al.Tomato SlERF. A1, SlERF. B4, SlERF. C3 and SlERF. A3, members of B3 group of ERF Family, are required for resistance to Botrytis cinerea[J]. Frontiers in Plant Science, 2016, 7:1964.
[78] Van der Does D, Leon-Reyes A, Koornneef A, et al. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59[J]. The Plant Cell, 2013, 25:744-761.
[79] Caarls L, Elberse J, Awwanah M, et al.Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114:6388-6393.
[80] Smirnova E, Marquis V, Poirier L, et al.Jasmonic acid oxidase 2 hydroxylates jasmonic acid and represses basal defense and resistance responses against Botrytis cinerea Infection[J]. Molecular Plant, 2017, 10:1159-1173.
[81] Du M, Zhao J, Tzeng DTW, et al.MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato[J]. The Plant Cell, 2017, 29:1883-1906.
[82] Lai Z, Wang F, Zheng Z, et al.A critical role of autophagy in plant resistance to necrotrophic fungal pathogens[J]. The Plant Journal, 2011, 66:953-968.
[83] Kabbage M, Kessens R, Dickman MB.A plant Bcl-2-associated athanogene is proteolytically activated to confer fungal resistance[J]. Microb Cell, 2016, 3:224-226.
[84] Li Y, Kabbage M, Liu W, et al.Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants[J]. The Plant Cell, 2016, 28:233-247.
[85] Li X, Zhang H, Tian L, et al.Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress[J]. Frontiers in Plant Science, 2015, 6:463.
[86] Survila M, Davidsson PR, Pennanen V, et al.Peroxidase-generated apoplastic ROS impair cuticle integrity and contribute to DAMP-elicited defenses[J]. Frontiers in Plant Science, 2016, 7:1945.
[87] Bi FC, Liu Z, Wu JX, et al.Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H₂O₂ bursts[J]. The Plant Cell, 2014, 26:3449-3467.
[88] Rossi FR, Krapp AR, Bisaro F, et al.Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea[J]. The Plant Journal:for Cell and Molecular Biology, 2017, 92:761-773.
[89] Mao G, Meng X, Liu Y, et al.Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis[J]. The Plant Cell, 2011, 23:1639-1653.
[90] Khare D, Choi H, Huh SU, et al.Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114:E5712-E5720.
[91] Burow M, Halkier BA, Kliebenstein DJ.Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness[J]. Current Opinion in Plant Biology, 2010, 13:348-353.
[92] Fan J, Doerner P.Genetic and molecular basis of nonhost disease resistance:complex, yes;silver bullet, no[J]. Current Opinion in Plant Biology, 2012, 15:400-406.
[93] Zhang Y, Zhang Y, Qiu D, et al.BcGs1, a glycoprotein from Botrytis cinerea, elicits defence response and improves disease resistance in host plants[J]. Biochemical and Biophysical Research Communications, 2015, 457:627-634.
[94] Xu J, Meng J, Meng X, et al.Pathogen-Responsive MPK3 and MPK6 reprogram the biosynthesis of indole glucosinolates and their derivatives in Arabidopsis immunity[J]. The Plant Cell, 2016, 28:1144-1162.
[95] Zhang Y, Jin X, Ouyang Z, et al.Vitamin B6 contributes to disease resistance against Pseudomonas syringae pv. tomato DC3000 and Botrytis cinerea in Arabidopsis thaliana[J]. Journal of Plant Physiology, 2015, 175:21-25.
[96] Lemonnier P, Gaillard C, Veillet F, et al.Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea[J]. Plant Molecular Biology, 2014, 85:473-484.
[97] Rizzi YS, Cecchini NM, Fabro G, et al.Differential control and function of Arabidopsis ProDH1 and ProDH2 genes on infection with biotrophic and necrotrophic pathogens[J]. Molecular Plant Pathology, 2017, 18:1164-1174.
[98] Zhao P, Zhang F, Liu D, et al.Matrix metalloproteinases operate redundantly in Arabidopsis immunity against necrotrophic and biotrophic fungal pathogens[J]. PLoS One, 2017, 12:e0183577.
[99] Li D, Zhang H, Song Q, et al.Tomato Sl3-MMP, a member of the Matrix metalloproteinase family, is required for disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000[J]. BMC Plant Biology, 2015, 15:143.
[100] Camanes G, Scalschi L, Vicedo B, et al.An untargeted global metabolomic analysis reveals the biochemical changes underlying basal resistance and priming in Solanum lycopersicum, and identifies 1-methyltryptophan as a metabolite involved in plant responses to Botrytis cinerea and Pseudomonas syringae[J]. The Plant Journal, 2015, 84:125-139.
[101] Zhang H, Hong Y, Huang L, et al.Virus-Induced gene silencing-based functional analyses revealed the involvement of several putative trehalose-6-phosphate synthase/phosphatase genes in disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 in tomato[J]. Frontiers in Plant Science, 2016, 7:1176.
[102] Polturak G, Grossman N, Vela-Corcia D, et al.Engineered gray mold resistance, antioxidant capacity, and pigmentation in betalain-producing crops and ornamentals[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114:9062-9067.
[103] Yan X, Qiao H, Zhang X, et al.Analysis of the grape(Vitis vinifera L.)thaumatin-like protein(TLP)gene family and demonstration that TLP29 contributes to disease resistance[J]. Scientific Reports, 2017, 7:4269.
[104] Wang Y, Wang D, Wang F, et al. Expression of the grape VaSTS19 Gene in Arabidopsis improves resistance to powdery mildew and Botrytis cinerea but increases susceptibility to Pseudomonas syringe pv tomato DC3000[J]. Int J Mol Sci, 2017, 18(9). pii:E2000.
[105] Huang L, Zhang S, Singer SD, et al.Expression of the Grape VqSTS21 Gene in Arabidopsis confers resistance to osmotic stress and biotrophic pathogens but not Botrytis cinerea[J]. Frontiers in Plant Science, 2016, 7:1379.
[106] Cerrudo I, Keller MM, Cargnel MD, et al.Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism[J]. Plant Physiology, 2012, 158:2042-2052.
[107] Cargnel MD, Demkura PV, Ballare CL.Linking phytochrome to plant immunity:low red:far-red ratios increase Arabidopsis susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin[J]. The New Phytologist, 2014, 204:342-354.
[108] Costa A, Barbaro MR, Sicilia F, et al.AIR12, a b-type cytochrome of the plasma membrane of Arabidopsis thaliana is a negative regulator of resistance against Botrytis cinerea[J]. Plant Sci, 2015, 233:32-43.
[109] Gommers CM, Keuskamp DH, Buti S, et al.Molecular profiles of contrasting shade response strategies in wild plants:differential control of immunity and shoot elongation[J]. The Plant Cell, 2017, 29:331-344.
[110] Mhamdi A, Noctor G.High CO₂ primes plant biotic stress defences through redox-linked pathways[J]. Plant Physiology, 2016, 172:929-942.
[111] Tomas-Grau RH, Requena-Serra FJ, Hael-Conrad V, et al.Soft mechanical stimulation induces a defense response against Botrytis cinerea in strawberry[J]. Plant Cell Reports, 2018, 37:239-250.
[112] Garcia T, Gutierrez J, Veloso J, et al.Wounding induces local resistance but systemic susceptibility to Botrytis cinerea in pepper plants[J]. Journal of Plant Physiology, 2015, 176:202-209.
[113] Tripathi D, Zhang T, Koo AJ, et al.Extracellular ATP acts on jasmonate signaling to reinforce plant defense[J]. Plant Physiology, 2017, 176:511-523.
[114] Segarra G, Santpere G, Elena G, et al.Enhanced Botrytis cinerea resistance of Arabidopsis plants grown in compost may be explained by increased expression of defense-related genes, as revealed by microarray analysis[J]. PLoS One, 2013, 8:e56075.
[115] Nie P, Li X, Wang S, et al.Induced systemic resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-dependent signaling pathway and activates PAMP-triggered immunity in Arabidopsis[J]. Frontiers in Plant Science, 2017, 8:238.
[116] Martinez-Hidalgo P, Garcia JM, Pozo MJ.Induced systemic resistance against Botrytis cinerea by Micromonospora strains isolated from root nodules[J]. Frontiers in Microbiology, 2015, 6:922.
[117] Sanchez-Bel P, Troncho P, Gamir J, et al.The nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato[J]. Front Microbiol, 2016, 7:1598.
[118] Miotto-Vilanova L, Jacquard C, Courteaux B, et al.Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization[J]. Front Plant Sci, 2016, 7:1236.
[119] Sharifi R, Ryu CM.Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both?[J]. Frontiers in Microbiology, 2016, 7:196.
[120] Noda J, Brito N, Gonzalez C.The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity[J]. BMC Plant Biol, 2010, 10:38.
[121] Frias M, Brito N, Gonzalez C.The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance(SAR)in tobacco and generates a wave of salicylic acid expanding from the site of application[J]. Molecular Plant Pathology, 2013, 14:191-196.
[122] Zhu W, Ronen M, Gur Y, et al.BcXYG1, a Secreted Xyloglucan-ase from Botrytis cinerea, triggers both cell death and plant immune responses[J]. Plant Physiology, 2017, 175:438-456.
[123] Ouyang Z, Li X, Huang L, et al.Elicitin-like proteins Oli-D1 and Oli-D2 from Pythium oligandrum trigger hypersensitive response in Nicotiana benthamiana and induce resistance against Botrytis cinerea in tomato[J]. Mol Plant Pathol, 2015, 16:238-250.
[124] Weiberg A, Wang M, Lin FM, et al.Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways[J]. Science, 2013, 342:118-123.
[125] Wang M, Weiberg A, Lin FM, et al.Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection[J]. Nature Plants, 2016, 2:16151.