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The complexity of the Sclerotinia sclerotiorum pathosystem in soybean: virulence factors, resistance mechanisms, and their exploitation to control Sclerotinia stem rot

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Abstract

Sclerotinia stem rot (SSR), caused by Sclerotinia sclerotiorum, is a globally important, yield limiting disease of soybean. Progress has been made in our understanding of this pathosystem at the plant level, such as the key role of oxalic acid in disease development and the importance of cell wall-degrading enzymes and other secreted proteins. Unfortunately, advances have largely focused on the fungal side of this interaction and only provide glimpses into the plant mechanisms governing resistance to this pathogen. With the absence of commercially available resistant soybeans, chemical and cultural solutions are being used by farmers to manage SSR with limited success. Additional research is needed to identify S. sclerotiorum resistance mechanisms that can be exploited to improve genetic resistance in soybean and decrease reliance on spray regimes. Technologies such as transgenics and RNAi could be exploited to improve the level of resistance to S. sclerotiorum in soybean. This review offers insight into the hurdles of managing SSR at the plant level and potential solutions that might be adopted in the future.

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Abbreviations

BiFC:

Bimolecular fluorescence complementation

CAZymes:

carbohydrate active enzymes

Chs:

chitin synthase

CWDE:

cell wall-degrading enzymes

DSI:

disease severity index

dsRNA:

double-stranded RNA

HIGS:

host-induced gene silencing

HR:

hypersensitive response

MAS:

marker assisted selection

OxDC:

oxalate decarboxylase

OxO:

oxalate oxidase

OA:

oxalic acid

sRNA:

small RNA

SSR:

Sclerotinia stem rot

PG:

endopolygalacturonases

OAH:

oxaloacetate acetylhydrolase

PGIP:

polygalacturonase-inhibiting protein

QTL:

quantitative trait loci

RIL:

recombinant inbred lines

RNAi:

RNA interference

ROS:

reactive oxygen species

siRNA:

small interfering RNA

SIGS:

spray-induced gene silencing

VIGS:

virus-induced gene silencing

References

  • Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier J‐M, Quévillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, Brault B, Chen Z, Choquer M, Collémare J, Cotton P, Danchin EG, Da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Güldener U, Henrissat B, Howlett B, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuvéglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Ségurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun M‐H, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics 7:e1002230

  • Andrade CM, Tinoco MLP, Rieth AF, Maia FCO, Aragão FJL (2016) Host-induced gene silencing in the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Plant Pathology 65:626–632

    Article  CAS  Google Scholar 

  • Arahana VS, Graef GL, Specht JE, Steadman JR, Eskridge KM (2001) Identification of QTLs for resistance to in soybean. Crop Science 41:180–188

    Article  CAS  Google Scholar 

  • Arias RS, Dang PM, Sobolev VS (2015) RNAi-mediated control of aflatoxins in peanut: method to analyze mycotoxin production and transgene expression in the peanut/Aspergillus pathosystem. Journal of Visualized Experiments: JoVE 106

  • Asoufi H, Hameed KM, Mahasneh A (2007) The cellulase and pectinase activities associated with the virulence of indigenous Sclerotinia sclerotiorum isolates in Jordan Valley. The Plant Pathology Journal 23:233–238

  • Bastien M, Sonah H, Belzile F (2014) Genome wide association mapping of resistance in soybean with a genotyping-by-sequencing approach. The Plant Genome 7:1–13

  • Bateman DF, Beer SV (1965) Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotium rolfsii. Phytopathology 55:204–211

    CAS  PubMed  Google Scholar 

  • Boland GJ, Hall R (1987) Evaluating soybean cultivars for resistance to Sclerotinia sclerotiorum under field conditions. Plant Disease 71:934–936

    Article  Google Scholar 

  • Bourras S, McNally KE, Müller MC, Wicker T, Keller B (2016) Avirulence genes in cereal powdery mildews: the gene-for-gene hypothesis 2.0. Frontiers in Plant Science 7:241

  • Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. The Plant Cell 12:2191–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang HX, Sang H, Wang J, McPhee KE, Zhuang X, Porter LD, Chilvers MI (2018) Exploring the genetics of lesion and nodal resistance in pea (Pisum sativum L.) to Sclerotinia sclerotiorum using genome-wide association studies and RNA-Seq. Plant Direct 2:e00064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Harel A, Gorovoits R, Yarden O, Dickman MB (2004) MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing. Molecular Plant-Microbe Interactions 17:404–413

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Kastner C, Nowara D, Oliveira-Garcia E, Rutten T, Zhao Y, Deising HB, Kumlehn J, Schweizer P (2016) Host-induced silencing of Fusarium culmorum genes protects wheat from infection. Journal of Experimental Botany 67:4979–4991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng W, Song XS, Li HP, Cao LH, Sun K, Qiu XL, Xu YB, Yang P, Huang T, Zhang JB, Qu B (2015) Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnology Journal 13:1335–1345

  • Cline MN, Jacobsen BJ (1983) Methods for evaluating soybean cultivars for resistance to Sclerotinia sclerotiorum. Plant Disease 67:784–786

    Article  Google Scholar 

  • Cober ER, Rioux S, Rajcan I, Donaldson PA, Simmonds DH (2003) Partial resistance to white mold in a transgenic soybean line. Crop Science 43:92

    Article  Google Scholar 

  • Conley SP, Roth AC, Gaska JM, and Smith DL (2017) 2017 Wisconsin soybean performance trials. Departments of Plant Pathology and Agronomy, University of Wisconsin, Madison. Retrieved from coolbean.info: http://www.coolbean.info/library/documents/2017_Soybean_VT_FINAL.pdf

  • Cunha WG, Tinoco MLP, Pancoti HL, Ribeiro RE, Aragão FJL (2010) High resistance to Sclerotinia sclerotiorum in transgenic soybean plants transformed to express an oxalate decarboxylase gene. Plant Pathology 59:654–660

    Article  CAS  Google Scholar 

  • Curtis MJ, Wolpert TJ (2002) The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant Journal 29:295–312

    Article  PubMed  Google Scholar 

  • De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Current Opinion in Plant Biology 5:295–299

    Article  PubMed  Google Scholar 

  • Del Rio L, Kurtzweil NC, Grau CR (2001) Petiole inoculation as a tool to screen soybean germ plasm for resistance to Sclerotinia sclerotiorum. (Abstract) Phytopathology 91:S176

    Google Scholar 

  • Derbyshire M, Denton-Giles M, Hegedus D, Seifbarghy S, Rollins J, van Kan J, Seidl MF, Faino L, Mbengue M, Navaud O, Raffaele S, Hammond-Kosack K, Heard S, Oliver R (2017) The complete genome sequence of the phytopathogenic fungus Sclerotinia sclerotiorum reveals insights into the genome architecture of broad host range pathogens. Genome Biology and Evolution 9:593–618

  • Derbyshire MC, Mbengue M, Barascud M, Navaud O, Raffaele S (2018) Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight candidate host target genes associated with quantitative disease resistance. bioRxiv 1:354076

    Google Scholar 

  • Dickman MB, Mitra A (1992) Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiological and Molecular Plant Pathology 41:255–263

    Article  Google Scholar 

  • Donaldson PA, Anderson T, Lane BG, Davidson AL, Simmonds DH (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiological Molecular Plant Pathology 59:297–307

    Article  CAS  Google Scholar 

  • Dumas B, Sailland A, Cheviet JP, Freyssinet G, Pallett K (1993) Identification of barley oxalate oxidase as a germin-like protein. Comptes Rendus de l'Academie des Sciences. Serie III, Sciences de la Vie 316:793–798

    CAS  Google Scholar 

  • Dutton MV, Evans CS (1996) Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Canadian Journal of Microbiology 42:881–895

    Article  CAS  Google Scholar 

  • Ghag SB, Shekhawat UK, Ganapathi TR (2014) Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against fusarium wilt in banana. Plant Biotechnology Journal 12:541–553

    Article  CAS  PubMed  Google Scholar 

  • Girard IJ, Tong C, Becker MG, Mao X, Huang J, de Kievit T, Fernando WD, Liu S, Belmonte MF (2017) RNA sequencing of Brassica napus reveals cellular redox control of Sclerotinia infection. Journal of Experimental Botany 68:5079–5091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godoy G, Steadman JR, Dickman MB, Dam R (1990) Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiological and Molecular Plant Pathology 37:179–191

    Article  CAS  Google Scholar 

  • Grau CR, Radke VL, Gillespie FL (1982) Resistance of soybean cultivars to Sclerotinia sclerotiorum. Plant Disease 66:506–508

    Article  Google Scholar 

  • Guo X, Wang D, Gordon SG, Helliwell E, Smith T, Berry SA, Dorrance AE (2008) Genetic mapping of QTLs underlying partial resistance to in soybean PI 391589A and PI 391589B. Crop Science 48:1129–1139

    Article  Google Scholar 

  • Guyon K, Balagué C, Roby D, Raffaele S (2014) Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15:336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han F, Katt M, Schuh W, and Webb DM (2008) QTL controlling Sclerotinia stem rot resistance in soybean. U.S. Patent 7250,552. Date issued: 18 September

  • Hu Z, Parekh U, Maruta N, Trusov Y, Botella JR (2015) Down-regulation of Fusarium oxysporum endogenous genes by host-delivered RNA interference enhances disease resistance. Frontiers in Chemistry 3:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huynh TT, Bastien M, Iquira E, Turcotte P, Belzile F (2010) Identification of QTLs associated with partial resistance to white mold in soybean using field-based inoculation. Crop Science 50:969–979

    Article  Google Scholar 

  • Huzar-Novakowiski J, Dorrance AE (2018) Ascospore inoculum density and characterization of components of partial resistance to Sclerotinia sclerotiorum in soybean. Plant Disease 102:1326–1333

  • Iquira E, Humira S, François B (2015) Association mapping of QTLs for Sclerotinia stem rot resistance in a collection of soybean plant introductions using a genotyping by sequencing (GBS) approach. BMC Plant Biology 15:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Joshi RK, Megha S, Rahman MH, Basu U, Kav NN (2016) A global study of transcriptome dynamics in canola (Brassica napus L.) responsive to Sclerotinia sclerotiorum infection using RNA-Seq. Gene 590:57–67

    Article  CAS  PubMed  Google Scholar 

  • Kabbage M, Williams B, Dickman MB (2013) Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathogens 9:e1003287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabbage M, Yarden O, Dickman MB (2015) Pathogenic attributes of Sclerotinia sclerotiorum: switching from a biotrophic to necrotrophic lifestyle. Plant Science 233:53–60

    Article  CAS  PubMed  Google Scholar 

  • Kesarwani M, Azam M, Natarajan K, Mehta A, Datta A (2000) Oxalate decarboxylase from Collybia velutipes molecular cloning and its overexpression to confer resistance to fungal infection in transgenic tobacco and tomato. Journal of Biological Chemistry 275:7230–7238

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Diers BW (2000) Inheritance of partial resistance to sclerotinia stem rot in soybean research supported by the Michigan Agricultural Experiment Station and grants from the Michigan Soybean Promotion Committee. Crop Science 40:55–61

    Article  Google Scholar 

  • Kim HS, Sneller CH, Diers BW (1999) Evaluation of soybean cultivars for resistance to Sclerotinia stem rot in field environments. Crop Science 39:64

    Article  Google Scholar 

  • Kim KS, Min JY, Dickman MB (2008) Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Molecular Plant-Microbe Interactions 21:605–612

    Article  CAS  PubMed  Google Scholar 

  • Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel KH (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to fusarium species. Proceedings of the National Academy of Sciences 110:19324–19329

    Article  CAS  Google Scholar 

  • Kotchoni SO, Gachomo EW (2006) The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. Journal of Biosciences 31:389–404

    Article  CAS  PubMed  Google Scholar 

  • Kubicek CP, Starr TL, Glass NL (2014) Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi. Annual Review of Phytopathology 52:427–451

    Article  CAS  PubMed  Google Scholar 

  • Kurian P, Stelzig DA (1979) The synergistic role of oxalic acid and endopolygalacturonase in bean leaves infected by Cristulariella pyramidalis. Phytopathology 69:1301–1304

    Article  CAS  Google Scholar 

  • Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. Journal of Biological Chemistry 268:12239–12242

    CAS  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Li D, Sun M, Han Y, Teng W, Li W (2010) Identification of QTL underlying soluble pigment content in soybean stems related to resistance to soybean white mold (Sclerotinia sclerotiorum). Euphytica 172:49–57

    Article  Google Scholar 

  • Liang HJ, Di YL, Li JL, Zhu FX (2015) Baseline sensitivity and control efficacy of fluazinam against Sclerotinia sclerotiorum. European Journal of Plant Pathology 142:691–699

    Article  CAS  Google Scholar 

  • Liang X, Liberti D, Li M, Kim YT, Hutchens A, Wilson R, Rollins JA (2015a) Oxaloacetate acetylhydrolase gene mutants of Sclerotinia sclerotiorum do not accumulate oxalic acid, but do produce limited lesions on host plants. Molecular Plant Pathology 16:559–571

    Article  CAS  PubMed  Google Scholar 

  • Liang X, Moomaw EW, Rollins JA (2015b) Fungal oxalate decarboxylase activity contributes to Sclerotinia sclerotiorum early infection by affecting both compound appressoria development and function. Molecular Plant Pathology 16:825–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R, McDonald MC, McDonald BA, Solomon PS, Lu S, Shelver WL, Xu S, Friesen TL (2012) The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathogens 8:e1002467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lumsden RD (1969) Sclerotinia sclerotiorum infection of bean and the production of cellulase. Phytopathology 59:653–657

    CAS  Google Scholar 

  • Lyu X, Shen C, Fu Y, Xie J, Jiang D, Li G, Cheng J (2016) A small secreted virulence-related protein is essential for the necrotrophic interactions of Sclerotinia sclerotiorum with its host plants. PLoS Pathogens 12:e1005435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masanga JO, Matheka JM, Omer RA, Ommeh SC, Monda EO, Alakonya AE (2015) Downregulation of transcription factor aflR in Aspergillus flavus confers reduction to aflatoxin accumulation in transgenic maize with alteration of host plant architecture. Plant Cell Reports 34:1379–1387

    Article  CAS  PubMed  Google Scholar 

  • McCaghey MM, Willbur J, Ranjan A, Grau CR, Chapman S, Diers B, Groves C, Kabbage M, Smith DL (2017) Development and evaluation of Glycine max germplasm lines with quantitative resistance to Sclerotinia sclerotiorum. Frontiers in Plant Science 8:1495

    Article  PubMed  PubMed Central  Google Scholar 

  • McLoughlin AG, Wytinck N, Walker PL, Girard IJ, Rashid KY, Kievit T, Fernando WD, Whyard S, Belmonte MF (2018) Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Scientific Reports 8:7320

  • Miklas PN, Grafton KF (1992) Inheritance of partial resistance to white mold in inbred populations of dry bean. Crop Science 32:943–948

    Article  Google Scholar 

  • Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GM, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nature Plants 3:16207

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends in Plant Science 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mochama P, Jadhav P, Neupane A, Marzano SY (2018) Mycoviruses as triggers and targets of RNA silencing in white mold fungus Sclerotinia sclerotiorum. Viruses 10:214

    Article  CAS  PubMed Central  Google Scholar 

  • Moellers TC, Singh A, Zhang J, Brungardt J, Kabbage M, Mueller DS, Grau CR, Ranjan A, Smith DL, Chowda-Reddy RV, Singh AK (2017) Main and epistatic loci studies in soybean for Sclerotinia sclerotiorum resistance reveal multiple modes of resistance in multi-environments. Scientific Reports 7:3554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munir E, Yoon JJ, Tokimatsu T, Hattori T, Shimada M (2001) New role for glyoxylate cycle enzymes in wood-rotting basidiomycetes in relation to biosynthesis of oxalic acid. Journal of Wood Science 47:368–373

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiology 164:1636–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. The Plant Cell 22:3130–3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira MB, de Andrade RV, Grossi-de-Sá MF, Petrofeza S (2015) Analysis of genes that are differentially expressed during the Sclerotinia sclerotiorumPhaseolus vulgaris interaction. Frontiers in Microbiology 6:1162

    PubMed  PubMed Central  Google Scholar 

  • Pérès (1995) Sclerotinia du soja: Premières évaluations du comportment variétal. CETIOM-Oléoscope 26:28–29

    Google Scholar 

  • Petrov VD, Van Breusegem F (2012) Hydrogen peroxide- a central hub for information flow in plant cells. AoB Plants 289:8735–8741

  • Prade RA, Zhan D, Ayoubi P, Mort AJ (1999) Pectins, pectinases and plant-microbe interactions. Biotechnology and Genetic Engineering Reviews 16:361–392

    Article  CAS  PubMed  Google Scholar 

  • Qi T, Zhu X, Tan C, Liu P, Guo J, Kang Z, Guo J (2017) Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnology Journal 16:797–807

  • Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 10:417–430

    Article  CAS  PubMed  Google Scholar 

  • Rafiqi M, Ellis JG, Ludowici VA, Hardham AR, Dodds PN (2012) Challenges and progress towards understanding the role of effectors in plant–fungal interactions. Current Opinion in Plant Biology 15:477–482

    Article  CAS  PubMed  Google Scholar 

  • Ranjan A, Jayaraman D, Grau C, Hill JH, Whitham SA, Ané JM, Smith DL, Kabbage M (2018) The pathogenic development of Sclerotinia sclerotiorum in soybean requires specific host NADPH oxidases. Molecular Plant Pathology 19:700–714

    Article  CAS  PubMed  Google Scholar 

  • Riou C, Freyssinet G, Fevre M (1991) Production of cell wall-degrading enzymes by the phytopathogenic fungus Sclerotinia sclerotiorum. Applied Environmental Microbiology 57:1478–1484

    CAS  PubMed  Google Scholar 

  • Rollins JA (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Molecular Plant-Microbe Interactions 16:785–795

    Article  CAS  PubMed  Google Scholar 

  • Rollins JA, Dickman MB (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Applied and Environmental Microbiology 67:75–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousseau G, Huynh Thanh T, Dostaler D, Rioux S (2004) Greenhouse and field assessments of resistance in soybean inoculated with sclerotia, mycelium, and ascospores of Sclerotinia sclerotiorum. Canadian Journal of Plant Science 84:615–623

    Article  Google Scholar 

  • Sebastian SA, Lu H, Han F, Kyle D, and Hedges BR (2010). Genetic loci associated with Sclerotinia tolerance in soybean. Unites States Patent 7,790,949 B2. Date issued: 7 September

  • Seifbarghi S, Borhan MH, Wei Y, Coutu C, Robinson SJ, Hegedus DD (2017) Changes in the Sclerotinia sclerotiorum transcriptome during infection of Brassica napus. BMC Genomics 18:266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Frontiers in Plant Science 7:187

    Article  PubMed  PubMed Central  Google Scholar 

  • Song Y, Thomma BP (2018) Host-induced gene silencing compromises Verticillium wilt in tomato and Arabidopsis. Molecular Plant Pathology 19:77–89

    Article  CAS  PubMed  Google Scholar 

  • SoyBase (2010) the USDA-ARS soybean genetics and genomics database. http://soybase.org

  • Uloth MB, Clode PL, You MP, Barbett MJ (2015) Calcium oxalate crystals: an integral component of the Sclerotinia sclerotiorum/Brassica carinata pathosystem. PLoS One 10:e0122362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vuong TD, Hoffman DD, Diers BW, Miller JF, Steadman JR, Hartman GL (2004) Evaluation of soybean, dry bean, and sunflower for resistance to Sclerotinia sclerotiorum. Crop Science 44:777–783

    Article  Google Scholar 

  • Vuong TD, Diers BW, Hartman GL (2008) Identification of QTL for resistance to Sclerotinia stem rot in soybean plant introduction 194639. Crop Science 48:2209

    Article  Google Scholar 

  • Wang M, Weiberg A, Lin FM, Thomma BP, Huang HD, Jin H (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nature Plants 2:16151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Molecular Biology 47:9–27

    Article  CAS  PubMed  Google Scholar 

  • Willbur JF, Ding S, Marks ME, Lucas H, Grau CR, Groves CL, Kabbage M, Smith DL (2017) Comprehensive Sclerotinia stem rot screening of soybean germplasm requires multiple isolates of Sclerotinia sclerotiorum. Plant Disease 101:344–353

    Article  CAS  PubMed  Google Scholar 

  • Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB (2011) Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathogens 7:e1002107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams SJ, Yin L, Foley G, Casey LW, Outram MA, Ericsson DJ, Lu J, Boden M, Dry IB, Kobe B (2016) Structure and function of the TIR domain from the grape NLR protein RPV1. Frontiers in Plant Science 7:1850

  • Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defense response. Acta Physiologiae Plantarum 19:581–589

    Article  CAS  Google Scholar 

  • Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. Journal of Experimental Botany 66:2839–2856

    Article  CAS  PubMed  Google Scholar 

  • Xiao X, Xie J, Cheng J, Li G, Yi X, Jiang D, Fu Y (2014) Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development. Molecular Plant-Microbe Interactions 40:40–55

    Article  CAS  Google Scholar 

  • Xu L, Xiang M, White D, Chen W (2015) pH dependency of sclerotial development and pathogenicity revealed by using genetically defined oxalate-minus mutants of Sclerotinia sclerotiorum. Environmental Microbiology 17:2896–2909

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Tang L, Gong Y, Xie J, Fu Y, Jiang D, Li G, Collinge DB, Chen W, Cheng J (2018) A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. New Phytologist 217:739–755

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Xiao J, Zhu W, Yang Y, Mei J, Bi C, Qian W, Qing L, Tan W (2017) Ss-Rhs1, a secretory Rhs repeat-containing protein, is required for the virulence of Sclerotinia sclerotiorum. Molecular Plant Pathology 18:1052–1061

    Article  CAS  PubMed  Google Scholar 

  • Zhao Z, Liu H, Wang C, Xu JR (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14:274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Han Y, Li Y, Liu D, Sun M, Zhao Y, Lv C, Li D, Yang Z, Huang L, Teng W (2015) Loci and candidate gene identification for resistance to Sclerotinia sclerotiorum in soybean (Glycine max L. Merr.) via association and linkage maps. The Plant Journal 82:245–255

    Article  CAS  PubMed  Google Scholar 

  • Zhou T, Boland GJ (1999) Mycelial growth and production of oxalic acid by virulent and hypovirulent isolates of Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology 21:93–99

    Article  CAS  Google Scholar 

  • Zhu W, Wei W, Fu Y, Cheng J, Xie J, Li G, Yi X, Kang Z, Dickman MB, Jiang D (2013) A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One 8:e53901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuppini A, Navazio L, Sella L, Castiglioni C, Favaron F, Mariani P (2005) An endopolygalacturonase from Sclerotinia sclerotiorum induces calcium-mediated signaling and programmed cell death in soybean cells. Molecular Plant-Microbe Interactions 18:849–855

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the funding sources that make our work and inquiry possible including the Wisconsin Soybean Marketing Board (WSMB), the North Central Soybean Research Program (NCSRP), SciMed at the University of Wisconsin-Madison, and the Department of Plant Pathology at University of Wisconsin-Madison.

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Correspondence to Mehdi Kabbage.

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Section Editor: Leandro J. Dallagnol

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McCaghey, M., Willbur, J., Smith, D.L. et al. The complexity of the Sclerotinia sclerotiorum pathosystem in soybean: virulence factors, resistance mechanisms, and their exploitation to control Sclerotinia stem rot. Trop. plant pathol. 44, 12–22 (2019). https://doi.org/10.1007/s40858-018-0259-4

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  • DOI: https://doi.org/10.1007/s40858-018-0259-4

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