A cosmopolitan fungal pathogen of dicots adopts an endophytic lifestyle on cereal crops and protects them from major fungal diseases

Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum , a widespread pathog...

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Published inThe ISME Journal Vol. 14; no. 12; pp. 3120 - 3135
Main Authors Tian, Binnian, Xie, Jiatao, Fu, Yanping, Cheng, Jiasen, Li, Bo, Chen, Tao, Zhao, Ying, Gao, Zhixiao, Yang, Puyun, Barbetti, Martin J., Tyler, Brett M., Jiang, Daohong
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.12.2020
Oxford University Press
Subjects
14/1
14/19
14/28
14/35
14/63
38/39
38/77
38/91
631/158/855
631/326/193/2539
82/1
82/51
Ascomycota
Biological control
Biomedical and Life Sciences
Blight
Cereal crops
Control methods
Crop yield
Disease resistance
Ecology
Ecosystem
Edible Grain
Endophytes
Evolutionary Biology
Food security
Fungal diseases
Fungi
Fusarium
Gene expression
Human populations
Humans
Life Sciences
Life Style
Magnoliopsida
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Microorganisms
Mycoses
Pathogens
Photosynthesis
Plant Diseases
Probiotics
Rice
Rice blast
Stripe rust
Wheat
Online AccessGet full text
ISSN1751-7362
1751-7370
1751-7370
DOI10.1038/s41396-020-00744-6

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Abstract Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum , a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4–18% in the field and consistently reduced Fusarium disease by 40–60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum , destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.
AbstractList Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4–18% in the field and consistently reduced Fusarium disease by 40–60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum, destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.
Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum , a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4–18% in the field and consistently reduced Fusarium disease by 40–60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum , destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.
Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4-18% in the field and consistently reduced Fusarium disease by 40-60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum, destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.Fungal pathogens are seriously threatening food security and natural ecosystems; efficient and environmentally friendly control methods are essential to help safeguard such resources for increasing human populations on a global scale. Here, we find that Sclerotinia sclerotiorum, a widespread pathogen of dicotyledons, can grow endophytically in wheat, rice, barley, maize, and oat, providing protection against Fusarium head blight, stripe rust, and rice blast. Protection is also provided by disabled S. sclerotiorum strains harboring a hypovirulence virus. The disabled strain DT-8 promoted wheat yields by 4-18% in the field and consistently reduced Fusarium disease by 40-60% across multiple field trials. We term the host-dependent trophism of S. sclerotiorum, destructively pathogenic or mutualistically endophytic, as schizotrophism. As a biotroph, S. sclerotiorum modified the expression of wheat genes involved in disease resistance and photosynthesis and increased the level of IAA. Our study shows that a broad-spectrum pathogen of one group of plants may be employed as a biocontrol agent in a different group of plants where they can be utilized as beneficial microorganisms while avoiding the risk of in-field release of pathogens. Our study also raises provocative questions about the potential role of schizotrophic endophytes in natural ecosystems.
Author Fu, Yanping
Barbetti, Martin J.
Li, Bo
Gao, Zhixiao
Cheng, Jiasen
Chen, Tao
Tian, Binnian
Yang, Puyun
Xie, Jiatao
Jiang, Daohong
Tyler, Brett M.
Zhao, Ying
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  organization: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, The Provincial Key Lab of Plant Pathology of Hubei Province, Huazhong Agricultural University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32814863$$D View this record in MEDLINE/PubMed
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PublicationSubtitle Multidisciplinary Journal of Microbial Ecology
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References CombyMLacosteSBaillieulFProfiziCDupontJSpatial and temporal variation of cultivable communities of co-occurring endophytes and pathogens in WheatFront Microb20167403
StauderCMNussDLZhangDXDoubleMLMacDonaldWLMethenyAMEnhanced hypovirus transmission by engineered super donor strains of the chestnut blight fungus, Cryphonectria parasitica, into a natural population of strains exhibiting diverse vegetative compatibility genotypesVirology2019528161:CAS:528:DC%2BC1cXisVyksb7I
HegedusDDRimmerSRSclerotinia sclerotiorum: when “to be or not to be” a pathogen?FEMS Microbiol Lett2005251177841:CAS:528:DC%2BD2MXhtVegu7rE
MaloyOCLangKJCarl Freiherr von Tubeuf: pioneer in biological control of plant diseasesAnnu Rev Phytopathol.20034141521:CAS:528:DC%2BD3sXptFWls7c%3D
YuXLiBFuYJiangDGhabrialSALiGA geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungusProc Natl Acad Sci USA20101078387921:CAS:528:DC%2BC3cXmtVWksr8%3D
BennettJWKlichMMycotoxinsClin Microbiol Rev2003164975161:CAS:528:DC%2BD3sXmsV2qtL4%3D
HuangHCChangCKozubGCEffect of temperature during sclerotial formation, sclerotial dryness, and relative humidity on myceliogenic germination of sclerotia of Sclerotinia sclerotiorumCan J Bot1998764949
AmselemJCuomoCAvan KanJAViaudMBenitoEPCoulouxAGenomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinereaPLoS Genet.20117e10022301:CAS:528:DC%2BC3MXhtFyhsb%2FK
FisherMCHenkDABriggsCJBrownsteinJSMadoffLCMcCrawSLEmerging fungal threats to animal, plant and ecosystem healthNature.2012484186941:CAS:528:DC%2BC38XmtVeqtb4%3D
KanehisaMArakiMGotoSHattoriMHirakawaMItohMKEGG for linking genomes to life and the environmentNucleic Acids Res200836D48041:CAS:528:DC%2BD1cXhtVSku7k%3D
XiaoJJinXJiaXWangHCaoAZhaoWTranscriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace WangshuibaiBMC Genom2013141:CAS:528:DC%2BC3sXot1yit7s%3D
ZhaoJWangMChenXKangZRole of alternate hosts in epidemiology and pathogen variation of cereal rustsAnnu Rev Phytopathol201654207281:CAS:528:DC%2BC28XpvV2ks78%3D
ChakrabortySNewtonACClimate change, plant diseases and food security: an overviewPlant Pathol201160214
HegewaldHWensch-DorendorfMSielingKChristenOImpacts of break crops and crop rotations on oilseed rape productivity: a reviewEur J Agron20181016377
DingSMehrabiRKotenCKangZWeiYSeongKTransducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearumEukaryot Cell20098867761:CAS:528:DC%2BD1MXotVyrs78%3D
KongLYangJLiGQiLZhangYWangCDifferent chitin synthase genes qre required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzaePLoS Pathog.20128e10025261:CAS:528:DC%2BC38XivVWgs7c%3D
ChristenOSielingKEffect of different preceding crops and crop rotations on yield of winter oil-seed rape (Brassica napus L.)J Agron Crop Sci199517426571
Agrios GN. Plant pathology. 5th ed. Elsevier Academic Press; Theobaldʼs Road, London WC1X 8RR, UK, 2005.
InoueYVyTTPYoshidaKAsanoHMitsuokaCAsukeSEvolution of the wheat blast fungus through functional losses in a host specificity determinantScience201735780831:CAS:528:DC%2BC2sXhtFans7bF
FravelDRCommercialization and implementation of biocontrolAnnu Rev Phytopathol200543337591:CAS:528:DC%2BD2MXhtVOksrvM
WebberJA natural biological control of Dutch elm diseaseNature198129244951
RedmanRSDuniganDDRodriguezRJFungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader?N Phytologist.200115170516
KeesingFBeldenLKDaszakPDobsonAHarvellCDHoltRDImpacts of biodiversity on the emergence and transmission of infectious diseasesNature2010468647521:CAS:528:DC%2BC3cXhsFSku7bE
DerbyshireMCDenton-GilesMThe control of sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunitiesPlant Pathol201665859771:CAS:528:DC%2BC28XhtFSqs7vK
HirumaKGerlachNSacristanSNakanoRTHacquardSKracherBRoot endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependentCell2016165464741:CAS:528:DC%2BC28XksVKrsb0%3D
FisherMCHawkinsNJSanglardDGurrSJWorldwide emergence of resistance to antifungal drugs challenges human health and food securityScience2018360739421:CAS:528:DC%2BC1cXpsVCgsbg%3D
LiYRenBDingLShenQPengSGuoSDoes chloroplast size influence photosynthetic nitrogen use efficiency?PLoS ONE20138e620361:CAS:528:DC%2BC3sXntVWjsbs%3D
DeanRVan KanJAPretoriusZAHammond-KosackKEDi PietroASpanuPDThe top 10 fungal pathogens in molecular plant pathologyMol Plant Pathol20121341430
BoltonMDThommaBPNelsonBDSclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogenMol Plant Pathol200671161:CAS:528:DC%2BD28Xit1yqs78%3D
LiuLXieJChengJFuYLiGYiXFungal negative-stranded RNA virus that is related to bornaviruses and nyavirusesProc Natl Acad Sci USA201411112205101:CAS:528:DC%2BC2cXht1Gqtb7N
SchillingerWFPaulitzTCCanola versus wheat rotation effects on subsequent wheat yieldField Crop Res20182232632
MortazaviAWilliamsBAMcCueKSchaefferLWoldBMapping and quantifying mammalian transcriptomes by RNA-SeqNat Methods.2008562181:CAS:528:DC%2BD1cXnslyqs7k%3D
GordonCSRajagopalanNRisseeuwEPSurpinMBallFJBarberCJCharacterization of Triticum aestivum abscisic acid receptors and a possible role for these in mediating Fusairum head blight susceptibility in wheatPLoS ONE.201611e0164996
GhabrialSACastonJRJiangDNibertMLSuzukiN50-plus years of fungal virusesVirology2015479-480356681:CAS:528:DC%2BC2MXjslynsLk%3D
XiongDYuTLiuXLiYPengSHuangJHeterogeneity of photosynthesis within leaves is associated with alteration of leaf structural features and leaf N content per leaf area in riceFunct Plant Biol2015426871:CAS:528:DC%2BC2MXps1Okurg%3D
QinLFuYXieJChengJJiangDLiGA nested-PCR method for rapid detection of Sclerotinia sclerotiorum on petals of oilseed rape (Brassica napus)Plant Pathol20116027171:CAS:528:DC%2BC3MXkvVGrtbc%3D
LiuHLiXXiaoJWangSA convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interactionPlant Methods201281:CAS:528:DC%2BC38Xjt1Krsro%3D
WangZGersteinMSnyderMRNA-Seq: a revolutionary tool for transcriptomicsNat Rev Genet20091057631:CAS:528:DC%2BD1cXhsFWis7bL
SinghRPHodsonDPHuerta-EspinoJJinYBhavaniSNjauPThe emergence of Ug99 races of the stem rust fungus is a threat to world wheat productionAnnu Rev Phytopathol201149465811:CAS:528:DC%2BC3MXhtFOhtrnM
ZhangXHalderJWhiteRPHughesDJYeZWangCClimate change increases risk of Fusarium ear blight on wheat in central ChinaAnn Appl Biol201416438495
AnagnostakisSLBiological control of chestnut blightScience1982215466711:STN:280:DC%2BC3cvislKitg%3D%3D
ZhangDXNussDLEngineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genesProc Natl Acad Sci USA2016113206271:CAS:528:DC%2BC28Xit12ktbs%3D
PfeiferMKuglerKGSandveSRZhanBRudiHHvidstenTRGenome interplay in the grain transcriptome of hexaploid bread wheatScience20143451250091
HarmanGEObregonMASamuelsGJLoritoMChanging models for commercialization and implementation of biocontrol in the developing and the developed worldPlant Dis.20109492839
ParkerIMSaundersMBontragerMWeitzAPHendricksRMagareyRPhylogenetic structure and host abundance drive disease pressure in communitiesNature201552054241:CAS:528:DC%2BC2MXotFaru74%3D
AshburnerMBallCABlakeJABotsteinDButlerHCherryJMGene ontology: tool for the unification of biology. The Gene Ontology ConsortiumNat Genet.2008252529
ArmstrongRDPerrisRMunnMDunsfordKRobertsonFHollawayGJEffects of long-term rotation and tillage practice on grain yield and protein of wheat and soil fertility on a Vertosol in a medium-rainfall temperate environmentCrop Pasture Sci20197011:CAS:528:DC%2BC1MXhvFGqsbs%3D
LeiLChenLShiXLiYWangJChenDA nodule-specific lipid transfer protein AsE246 participates in transport of plant-synthesized lipids to symbiosome membrane and is essential for nodule organogenesis in Chinese milk vetchPlant Physiol.20141641045581:CAS:528:DC%2BC2cXks1Slsrg%3D
XieJJiangDNew insights into mycoviruses and exploration for the biological control of crop fungal diseasesAnnu Rev Phytopathol20145245681:CAS:528:DC%2BC2cXhsl2msrfI
XuLLiGJiangDChenWSclerotinia sclerotiorum: an evaluation of virulence theoriesAnnu Rev Phytopathol201856311381:CAS:528:DC%2BC1cXht1Cjur%2FJ
WuFPerspective: time to face the fungal threatNature.2014516S71:CAS:528:DC%2BC2cXitFams7bE
Pfeifer (2024011300400900100_CR8) 2014; 345
Fravel (2024011300400900100_CR11) 2005; 43
Hegewald (2024011300400900100_CR19) 2018; 101
Fisher (2024011300400900100_CR9) 2018; 360
Inoue (2024011300400900100_CR7) 2017; 357
Armstrong (2024011300400900100_CR20) 2019; 70
Maloy (2024011300400900100_CR10) 2003; 41
Yu (2024011300400900100_CR21) 2010; 107
Zhang (2024011300400900100_CR38) 2014; 164
Ashburner (2024011300400900100_CR32) 2008; 25
Xiao (2024011300400900100_CR34) 2013; 14
Amselem (2024011300400900100_CR15) 2011; 7
Christen (2024011300400900100_CR16) 1995; 174
Agrios (2024011300400900100_CR1) 2005
Lei (2024011300400900100_CR23) 2014; 164
Parker (2024011300400900100_CR51) 2015; 520
Schillinger (2024011300400900100_CR18) 2018; 223
Bennett (2024011300400900100_CR2) 2003; 16
Dean (2024011300400900100_CR4) 2012; 13
Mortazavi (2024011300400900100_CR31) 2008; 5
Ghabrial (2024011300400900100_CR41) 2015; 479-480
Singh (2024011300400900100_CR6) 2011; 49
Xiong (2024011300400900100_CR25) 2015; 42
Li (2024011300400900100_CR26) 2013; 8
Gordon (2024011300400900100_CR35) 2016; 11
Chakraborty (2024011300400900100_CR37) 2011; 60
Comby (2024011300400900100_CR40) 2016; 7
Hegedus (2024011300400900100_CR48) 2005; 251
Stauder (2024011300400900100_CR46) 2019; 528
Wang (2024011300400900100_CR30) 2009; 10
Zhang (2024011300400900100_CR45) 2016; 113
Xu (2024011300400900100_CR13) 2018; 56
Kong (2024011300400900100_CR29) 2012; 8
Harman (2024011300400900100_CR12) 2010; 94
Kanehisa (2024011300400900100_CR33) 2008; 36
Fisher (2024011300400900100_CR5) 2012; 484
Hiruma (2024011300400900100_CR49) 2016; 165
Xie (2024011300400900100_CR44) 2014; 52
Keesing (2024011300400900100_CR50) 2010; 468
Wu (2024011300400900100_CR3) 2014; 516
Anagnostakis (2024011300400900100_CR43) 1982; 215
Liu (2024011300400900100_CR27) 2012; 8
Qin (2024011300400900100_CR24) 2011; 60
Huang (2024011300400900100_CR47) 1998; 76
Webber (2024011300400900100_CR42) 1981; 292
Derbyshire (2024011300400900100_CR17) 2016; 65
Liu (2024011300400900100_CR22) 2014; 111
Ding (2024011300400900100_CR28) 2009; 8
Bolton (2024011300400900100_CR14) 2006; 7
Redman (2024011300400900100_CR36) 2001; 151
Zhao (2024011300400900100_CR39) 2016; 54
References_xml – reference: LeiLChenLShiXLiYWangJChenDA nodule-specific lipid transfer protein AsE246 participates in transport of plant-synthesized lipids to symbiosome membrane and is essential for nodule organogenesis in Chinese milk vetchPlant Physiol.20141641045581:CAS:528:DC%2BC2cXks1Slsrg%3D
– reference: LiuHLiXXiaoJWangSA convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interactionPlant Methods201281:CAS:528:DC%2BC38Xjt1Krsro%3D
– reference: QinLFuYXieJChengJJiangDLiGA nested-PCR method for rapid detection of Sclerotinia sclerotiorum on petals of oilseed rape (Brassica napus)Plant Pathol20116027171:CAS:528:DC%2BC3MXkvVGrtbc%3D
– reference: BoltonMDThommaBPNelsonBDSclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogenMol Plant Pathol200671161:CAS:528:DC%2BD28Xit1yqs78%3D
– reference: XiaoJJinXJiaXWangHCaoAZhaoWTranscriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace WangshuibaiBMC Genom2013141:CAS:528:DC%2BC3sXot1yit7s%3D
– reference: FravelDRCommercialization and implementation of biocontrolAnnu Rev Phytopathol200543337591:CAS:528:DC%2BD2MXhtVOksrvM
– reference: WuFPerspective: time to face the fungal threatNature.2014516S71:CAS:528:DC%2BC2cXitFams7bE
– reference: XiongDYuTLiuXLiYPengSHuangJHeterogeneity of photosynthesis within leaves is associated with alteration of leaf structural features and leaf N content per leaf area in riceFunct Plant Biol2015426871:CAS:528:DC%2BC2MXps1Okurg%3D
– reference: GhabrialSACastonJRJiangDNibertMLSuzukiN50-plus years of fungal virusesVirology2015479-480356681:CAS:528:DC%2BC2MXjslynsLk%3D
– reference: SinghRPHodsonDPHuerta-EspinoJJinYBhavaniSNjauPThe emergence of Ug99 races of the stem rust fungus is a threat to world wheat productionAnnu Rev Phytopathol201149465811:CAS:528:DC%2BC3MXhtFOhtrnM
– reference: KongLYangJLiGQiLZhangYWangCDifferent chitin synthase genes qre required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzaePLoS Pathog.20128e10025261:CAS:528:DC%2BC38XivVWgs7c%3D
– reference: XieJJiangDNew insights into mycoviruses and exploration for the biological control of crop fungal diseasesAnnu Rev Phytopathol20145245681:CAS:528:DC%2BC2cXhsl2msrfI
– reference: MaloyOCLangKJCarl Freiherr von Tubeuf: pioneer in biological control of plant diseasesAnnu Rev Phytopathol.20034141521:CAS:528:DC%2BD3sXptFWls7c%3D
– reference: XuLLiGJiangDChenWSclerotinia sclerotiorum: an evaluation of virulence theoriesAnnu Rev Phytopathol201856311381:CAS:528:DC%2BC1cXht1Cjur%2FJ
– reference: SchillingerWFPaulitzTCCanola versus wheat rotation effects on subsequent wheat yieldField Crop Res20182232632
– reference: StauderCMNussDLZhangDXDoubleMLMacDonaldWLMethenyAMEnhanced hypovirus transmission by engineered super donor strains of the chestnut blight fungus, Cryphonectria parasitica, into a natural population of strains exhibiting diverse vegetative compatibility genotypesVirology2019528161:CAS:528:DC%2BC1cXisVyksb7I
– reference: FisherMCHenkDABriggsCJBrownsteinJSMadoffLCMcCrawSLEmerging fungal threats to animal, plant and ecosystem healthNature.2012484186941:CAS:528:DC%2BC38XmtVeqtb4%3D
– reference: KeesingFBeldenLKDaszakPDobsonAHarvellCDHoltRDImpacts of biodiversity on the emergence and transmission of infectious diseasesNature2010468647521:CAS:528:DC%2BC3cXhsFSku7bE
– reference: Agrios GN. Plant pathology. 5th ed. Elsevier Academic Press; Theobaldʼs Road, London WC1X 8RR, UK, 2005.
– reference: ChristenOSielingKEffect of different preceding crops and crop rotations on yield of winter oil-seed rape (Brassica napus L.)J Agron Crop Sci199517426571
– reference: WangZGersteinMSnyderMRNA-Seq: a revolutionary tool for transcriptomicsNat Rev Genet20091057631:CAS:528:DC%2BD1cXhsFWis7bL
– reference: LiYRenBDingLShenQPengSGuoSDoes chloroplast size influence photosynthetic nitrogen use efficiency?PLoS ONE20138e620361:CAS:528:DC%2BC3sXntVWjsbs%3D
– reference: FisherMCHawkinsNJSanglardDGurrSJWorldwide emergence of resistance to antifungal drugs challenges human health and food securityScience2018360739421:CAS:528:DC%2BC1cXpsVCgsbg%3D
– reference: BennettJWKlichMMycotoxinsClin Microbiol Rev2003164975161:CAS:528:DC%2BD3sXmsV2qtL4%3D
– reference: DerbyshireMCDenton-GilesMThe control of sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunitiesPlant Pathol201665859771:CAS:528:DC%2BC28XhtFSqs7vK
– reference: ZhaoJWangMChenXKangZRole of alternate hosts in epidemiology and pathogen variation of cereal rustsAnnu Rev Phytopathol201654207281:CAS:528:DC%2BC28XpvV2ks78%3D
– reference: AnagnostakisSLBiological control of chestnut blightScience1982215466711:STN:280:DC%2BC3cvislKitg%3D%3D
– reference: PfeiferMKuglerKGSandveSRZhanBRudiHHvidstenTRGenome interplay in the grain transcriptome of hexaploid bread wheatScience20143451250091
– reference: ParkerIMSaundersMBontragerMWeitzAPHendricksRMagareyRPhylogenetic structure and host abundance drive disease pressure in communitiesNature201552054241:CAS:528:DC%2BC2MXotFaru74%3D
– reference: HarmanGEObregonMASamuelsGJLoritoMChanging models for commercialization and implementation of biocontrol in the developing and the developed worldPlant Dis.20109492839
– reference: ArmstrongRDPerrisRMunnMDunsfordKRobertsonFHollawayGJEffects of long-term rotation and tillage practice on grain yield and protein of wheat and soil fertility on a Vertosol in a medium-rainfall temperate environmentCrop Pasture Sci20197011:CAS:528:DC%2BC1MXhvFGqsbs%3D
– reference: RedmanRSDuniganDDRodriguezRJFungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader?N Phytologist.200115170516
– reference: AmselemJCuomoCAvan KanJAViaudMBenitoEPCoulouxAGenomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinereaPLoS Genet.20117e10022301:CAS:528:DC%2BC3MXhtFyhsb%2FK
– reference: ChakrabortySNewtonACClimate change, plant diseases and food security: an overviewPlant Pathol201160214
– reference: LiuLXieJChengJFuYLiGYiXFungal negative-stranded RNA virus that is related to bornaviruses and nyavirusesProc Natl Acad Sci USA201411112205101:CAS:528:DC%2BC2cXht1Gqtb7N
– reference: KanehisaMArakiMGotoSHattoriMHirakawaMItohMKEGG for linking genomes to life and the environmentNucleic Acids Res200836D48041:CAS:528:DC%2BD1cXhtVSku7k%3D
– reference: GordonCSRajagopalanNRisseeuwEPSurpinMBallFJBarberCJCharacterization of Triticum aestivum abscisic acid receptors and a possible role for these in mediating Fusairum head blight susceptibility in wheatPLoS ONE.201611e0164996
– reference: DeanRVan KanJAPretoriusZAHammond-KosackKEDi PietroASpanuPDThe top 10 fungal pathogens in molecular plant pathologyMol Plant Pathol20121341430
– reference: AshburnerMBallCABlakeJABotsteinDButlerHCherryJMGene ontology: tool for the unification of biology. The Gene Ontology ConsortiumNat Genet.2008252529
– reference: HirumaKGerlachNSacristanSNakanoRTHacquardSKracherBRoot endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependentCell2016165464741:CAS:528:DC%2BC28XksVKrsb0%3D
– reference: WebberJA natural biological control of Dutch elm diseaseNature198129244951
– reference: DingSMehrabiRKotenCKangZWeiYSeongKTransducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearumEukaryot Cell20098867761:CAS:528:DC%2BD1MXotVyrs78%3D
– reference: ZhangDXNussDLEngineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genesProc Natl Acad Sci USA2016113206271:CAS:528:DC%2BC28Xit12ktbs%3D
– reference: MortazaviAWilliamsBAMcCueKSchaefferLWoldBMapping and quantifying mammalian transcriptomes by RNA-SeqNat Methods.2008562181:CAS:528:DC%2BD1cXnslyqs7k%3D
– reference: HegewaldHWensch-DorendorfMSielingKChristenOImpacts of break crops and crop rotations on oilseed rape productivity: a reviewEur J Agron20181016377
– reference: InoueYVyTTPYoshidaKAsanoHMitsuokaCAsukeSEvolution of the wheat blast fungus through functional losses in a host specificity determinantScience201735780831:CAS:528:DC%2BC2sXhtFans7bF
– reference: HuangHCChangCKozubGCEffect of temperature during sclerotial formation, sclerotial dryness, and relative humidity on myceliogenic germination of sclerotia of Sclerotinia sclerotiorumCan J Bot1998764949
– reference: CombyMLacosteSBaillieulFProfiziCDupontJSpatial and temporal variation of cultivable communities of co-occurring endophytes and pathogens in WheatFront Microb20167403
– reference: YuXLiBFuYJiangDGhabrialSALiGA geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungusProc Natl Acad Sci USA20101078387921:CAS:528:DC%2BC3cXmtVWksr8%3D
– reference: ZhangXHalderJWhiteRPHughesDJYeZWangCClimate change increases risk of Fusarium ear blight on wheat in central ChinaAnn Appl Biol201416438495
– reference: HegedusDDRimmerSRSclerotinia sclerotiorum: when “to be or not to be” a pathogen?FEMS Microbiol Lett2005251177841:CAS:528:DC%2BD2MXhtVegu7rE
– volume: 8
  start-page: 2
  year: 2012
  ident: 2024011300400900100_CR27
  article-title: A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction
  publication-title: Plant Methods
  doi: 10.1186/1746-4811-8-2
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Magnoliopsida
Microbial Ecology
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Stripe rust
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Title A cosmopolitan fungal pathogen of dicots adopts an endophytic lifestyle on cereal crops and protects them from major fungal diseases
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