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Over-expression of GmKR3, a TIR–NBS–LRR type R gene, confers resistance to multiple viruses in soybean

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That overexpression of GmKR3 enhances innate virus resistance by stimulating.

Abstract

Soybean mosaic virus (SMV) is found in many soybean production areas, and SMV infection is one of the prevalent viral diseases that can cause significant yield losses in soybean. In plants, resistance (R) genes are involved in pathogen reorganization and innate immune response activation. Most R proteins have nucleotide-binding site and leucine-rich repeat (NBS–LRR) domains, and some of the NBS–LRR type R proteins in dicots have Toll/Interleukin-1 Receptor (TIR) motifs. We report here the analysis of the over-expression of GmKR3, a soybean TIR–NBS–LRR type R gene on virus resistance in soybean. When over-expressed in soybean, GmKR3 enhanced the plant’s resistance to several strains of SMV, the closely related potyviruses bean common mosaic virus (BCMV) and watermelon mosaic virus (WMV), and the secovirus bean pod mottle virus (BPMV). Importantly, over-expression of GmKR3 did not affect plant growth and development, including yield and qualities of the seeds. HPLC analysis showed that abscisic acid (ABA) content increased in the 35S:GmKR3 transgenic plants, and in both wild-type and 35S:GmKR3 transgenic plants in response to virus inoculation. Consistent with this observation, we found that the expression of two ABA catabolism genes was down-regulated in 35S:GmKR3 transgenic plants. We also found that the expression of Gm04.3, an ABA responsive gene encoding BURP domain-containing protein, was up-regulated in 35S:GmKR3 transgenic plants. Taken together, our results suggest that overexpression of GmKR3 enhanced virus resistance in soybean, which was achieved at least in part via ABA signaling.

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References

  • Ahangaran A, Habibi MK, Mohammadi GH, Winter S, Garcia-Arenal F (2013) Analysis of Soybean mosaic virus genetic diversity in Iran allows the characterization of a new mutation resulting in overcoming Rsv4-resistance. Mol Plant Virol 94:2557–2568

    CAS  Google Scholar 

  • Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol 16:529–540

    Article  CAS  PubMed  Google Scholar 

  • Alazem M, Lin NS (2017) Antiviral roles of abscisic acid in plants. Front Plant Sci 8:1760

    Article  PubMed  PubMed Central  Google Scholar 

  • Alazem M, Lin KY, Lin NS (2015) The abscisic acid pathway has multifaceted effects on the accumulation of bamboo mosaic virus. Mol Plant Microbe Interact 27:177–189

    Article  CAS  Google Scholar 

  • Alazem M, He MH, Moffett P, Lin NS (2017) Abscisic acid induces resistance against bamboo mosaic virus through Argonaute 2 and 3. Plant Physiol 174:339–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Bio 7:391–399

    Article  CAS  Google Scholar 

  • Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M (2007) Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51:589–603

    Article  CAS  PubMed  Google Scholar 

  • Buzzell RI, Tu JC (1989) Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic virus. J Hered 80:400–401

    Article  Google Scholar 

  • Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant-pathogen interactions. J Plant Res 124:489–499

    Article  CAS  PubMed  Google Scholar 

  • Chen P, Ma G, Buss GR, Gunduz I, Roane CW, Tolin SA (2001) Inheritance and allelism tests of Raiden soybean for resistance to soybean mosaic virus. J Hered 92:51–55

    Article  CAS  PubMed  Google Scholar 

  • Chen LJ, Zou WS, Wu G, Lin HH, Xi DH (2018) Tobacco alpha-expansin EXPA4 plays a role in Nicotiana benthamiana defence against tobacco mosaic virus. Planta 247:355–368

    Article  CAS  PubMed  Google Scholar 

  • Cheng YQ, Liu ZM, Xu J, Zhou T, Wang M, Chen YT, Li HF, Fan ZF (2008) HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 in vitro and in planta. J Gen Virol 89:2046–2054

    Article  CAS  PubMed  Google Scholar 

  • Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467–470

    Article  Google Scholar 

  • Cho EK, Goodman RM (1982) Evaluation of resistance in soybeans to soybean mosaic virus strains. Crop Sci 22:1133–1136

    Article  Google Scholar 

  • Choi DS, Hwang BK (2011) Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 23:823–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collier SM, Moffett P (2009) NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–529

    Article  CAS  PubMed  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Day B, Dahlbeck D, Staskawicz BJ (2006) NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–2791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–965

    Article  CAS  PubMed  Google Scholar 

  • Desbiez C, Lecoq H (2004) The nucleotide sequence of watermelon mosaic virus (WMV, Potyvirus) reveals interspecific recombination between two related potyviruses in the 5′ part of the genome. Adv Virol 149:1619–1632

    CAS  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89:2480–2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16:449–455

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl 1):S15–S45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox CM, Kim KS, Cregan PB, Hill CB, Hartman GL, Diers BW (2014) Inheritance of soybean aphid resistance in 21 soybean plant introductions. Theor Appl Genet 127:43–50

    Article  CAS  PubMed  Google Scholar 

  • Fu S, Zhan Y, Zhi H, Gai J, Yu D (2006) Mapping of smv resistance gene rsc-7 by ssr markers in soybean. Genetica 128:63–69

    Article  CAS  PubMed  Google Scholar 

  • Fu DQ, Ghabrial S, Kachroo A (2009) GmRAR1 and GmSGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Mol Plant Microbe Interact 22:86–95

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Zhu JK, Jagendorf AT (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385

    Article  PubMed  PubMed Central  Google Scholar 

  • Furutani N, Hidaka S, Kosaka Y, Shizukawa Y, Kanematsu S (2006) Coat protein gene-mediated resistance to soybean mosaic virus in transgenic soybean. Breed Sci 56:119–124

    Article  CAS  Google Scholar 

  • Gunduz I, Buss GR, Chen P, Tolin SA (2002) Characterization of SMV resistance genes in Tousan 140 and Hourei soybean. Crop sci 42:90–95

    Article  PubMed  Google Scholar 

  • Guo J, Yang X, Weston DJ, Chen JG (2011) Abscisic acid receptors: past, present and future. J Integr Plant Biol 53:469–479

    Article  CAS  PubMed  Google Scholar 

  • Guttikonda SK, Trupti J, Bisht NC, Chen H, An YQ, Pandey S, Xu D, Yu O (2010) Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases. BMC Plant Biol 10:243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes AJ, Ma G, Buss GR, Maroof MAS (2000) Molecular marker mapping of RSV4, a gene conferring resistance to all known strains of soybean mosaic virus. Crop Sci 40:1434–1437

    Article  CAS  Google Scholar 

  • He H, Yang X, Xun H, Lou X, Li S, Zhang Z, Jiang L, Dong Y, Wang S, Pang J, Liu B (2017) Over-expression of GmSN1 enhances virus resistance in Arabidopsis and soybean. Plant Cell Rep 36:1441–1455

    Article  CAS  PubMed  Google Scholar 

  • Hu R, Fan C, Li H, Zhang Q, Fu YF (2009) Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Mol Biol 10:93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  CAS  PubMed  Google Scholar 

  • Irwin ME, Schultz GA (1981) Soybean mosaic virus. FAO Plant Prot Bull 29:41–55

    Google Scholar 

  • Kato S, Takada Y, Shimamura S, Hirata K, Sayama T, Taguchi-Shiobara F, Ishimoto M, Kikuchi A, Nishio T (2016) Transfer of the rsv3 locus from ‘harosoy’ for resistance to soybean mosaic virus strains c and d in Japan. Breeding Sci 66:319–327

    Article  CAS  Google Scholar 

  • Kiihl RAS, Hartwig EE (1979) Inheritance of reaction to soybean mosaic virus insoybeans1. Crop Sci 19:372–375

    Article  Google Scholar 

  • Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant Microbe Interact 20:120–128

    Article  CAS  PubMed  Google Scholar 

  • Koning G, Tekrony DM, Ghabrial SA, Pfeiffer TW (2002) Soybean mosaic virus (SMV) and the SMV resistance gene (Rsv1). Crop Sci 1:178–185

    Article  Google Scholar 

  • Kragler F, Curin M, Trutnyeva K, Gansch A, Waigmann E (2003) MPB2C, a microtubule-associated plant protein binds to and interferes with cell-to-cell transport of tobacco mosaic virus movement protein. Plant Physiol 132:1870–1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SY, Lee DH (2005) Expression of mbr4, a TIR-NBS type of apple r, gene, confers resistance to bacterial spot disease in Arabidopsis. J Plant Biol 48:220–228

    Article  CAS  Google Scholar 

  • Lee SY, Choi YJ, Ha YM, Lee DH (2007) Ectopic expression of apple Mbr7 gene induced enhanced resistance to transgenic Arabidopsis plant against a virulent pathogen. J Microbiol Biotechnol 17:130–137

    CAS  PubMed  Google Scholar 

  • Li K, Yang QH, Zhi HJ, Gai JY (2010) Identification and distribution of Soybean mosaic virus strains in Southern China. Plant Dis 94:351–357

    Article  CAS  PubMed  Google Scholar 

  • Li JF, Bush J, Xiong Y, Li L, McCormack M (2011) Large-scale protein–protein interaction analysis in Arabidopsis mesophyll protoplasts by split firefly luciferase complementation. Plos One 6:e27364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li K, Ren R, Adhimoolam K, Gao L, Yuan Y, Liu Z (2016) Genetic analysis and identification of two soybean mosaic virus resistance genes in soybean [glycine max (l.) merr]. Plant Breed 134:684–695

    Article  CAS  Google Scholar 

  • Liao F, Guo JZ, Liu Y, Huang GM, Liu YT, Liu P (2008) Progress on research on seed-transmitted beanpod mottle virus (BPMV) of soybean. China Plant Prot 28:11

    Google Scholar 

  • Liu JZ, Fang Y, Pang H (2016) The current status of the soybean-soybean mosaic virus (SMV) pathosystem. Front Microbiol 7:1906

    PubMed  PubMed Central  Google Scholar 

  • Luan H, Shine MB, Cui X, Chen X, Ma N, Kachroo P, Zhi H, Kachroo A (2016) The potyviral P3 protein targets eukaryotic elongation factor 1A to promote the unfolded protein response and viral pathogenesis. Plant Physiol 172:221–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma G, Chen P, Buss GR, Tolin SA (1995) Genetic characteristics of two genes for resistance to soybean mosaic virus in PI486355 soybean. Theor Appl Genet 91:907–914

    Article  CAS  PubMed  Google Scholar 

  • Maroof MAS, Tucker DM, Skoneczka JA, Bowman BC, Tripathy S, Tolin SA (2010) Fine mapping and candidate gene discovery of the soybean mosaic virus resistance gene, Rsv4. Plant Genome 3:14–22

    Article  CAS  Google Scholar 

  • Michael Weaver L, Swiderski MR, Li Y, Jones JD (2006) The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J 47:829–840

    Article  CAS  PubMed  Google Scholar 

  • Moeder W, Ung H, Mosher S, Yoshioka K (2010) SA-ABA antagonism in defense responses. Plant Signal Behav 5(10):1231–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 17:4511–4519

    Article  Google Scholar 

  • Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–2806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niehl A, Pena EJ, Amari K, Heinlein M (2013) Microtubules in viral replication and transport. Plant J 75:290–308

    Article  CAS  PubMed  Google Scholar 

  • Park S, Li F, Renaud J, Shen W, Li Y, Guo L, Cui H, Sumarah M, Wang A (2017) NbEXPA1, an α-Expansin, is plasmodesmata-specific and a novel host factor for potyviral infection. Plant J 92:846–861

    Article  CAS  PubMed  Google Scholar 

  • Paz MM, Shou H, Guo Z, Zhang Z, Banerjee AK, Wang K (2004) Assessment of conditions affecting agrobacterium-mediated soybean transformation using the cotyledonary node explants. Euphytica 136:167–179

    Article  CAS  Google Scholar 

  • Reddy MSS, Ghabrial SA, Redmond CT, Dinkins RD, Collins GB (2001) Resistance to bean pod mottle virus in transgenic soybean lines expressing the capsid polyprotein. Phytopathology 91:831–838

    Article  CAS  PubMed  Google Scholar 

  • Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koshiba T (2002) Complex regulation of aba biosynthesis in plants. Trends Plant Sci 7:41–48

    Article  CAS  PubMed  Google Scholar 

  • Seo JK, Kwon SJ, Cho WK, Choi HS, Kim KH (2014) Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Sci Rep 4:5905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shuai H, Meng Y, Luo X, Chen F, Zhou W, Dai Y (2017) Exogenous auxin represses soybean seed germination through decreasing the gibberellin/abscisic acid (ga/aba) ratio. Sci Rep 7:12620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song L, Huang SC, Wise A, Castanon R, Nery JR, Chen H, Watanabe M, Thomas J, Bar-Joseph Z, Ecker JR (2016) A transcription factor hierarchy defines an environmental stress response network. Science 354:aag1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staskawicz BJ, Dahlbeck D, Keen NT (1984) Cloned avirulence gene of pseudomonas syringae pv. glycinea determines race-specific incompatibility on glycine max (L.) merr. Proc Natl Acad Sci USA 81:6024–6028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su JS, Bowman BC, Jeong N, Yang K, Kastl C, Tolin SA, Maroof MAS, Jeong SC (2011) The Rsv3 locus conferring resistance to soybean mosaic virus is associated with a cluster of coiled-coil nucleotide-binding leucine-rich repeat genes. Plant Genome 4:55–64

    Article  Google Scholar 

  • Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB (1999) Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11:15–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tel-Zur N, Abbo S, Myslabodski D, Mizrahi Y (1999) Modified CTAB procedure for DNA isolation from epiphytic cacti of the genera Hylocereus and Selenicereus (Cactaceae). Plant Mol Bio Rep 17:249–254

    Article  CAS  Google Scholar 

  • Tian H, Guo H, Dai X, Cheng Y, Zheng K, Wang X, Wang S (2015) An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis. Sci Rep 5:17587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian H, Chen S, Yang W, Wang T, Zheng K, Wang Y, Cheng Y, Zhang N, Liu S, Li D, Liu B, Wang S (2017) A novel family of transcription factors conserved in angiosperms is required for ABA signalling. Plant Cell Environ 40:2958–2971

    Article  CAS  PubMed  Google Scholar 

  • Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317

    Article  CAS  PubMed  Google Scholar 

  • Tran PT, Widyasari K, Seo JK, Kim KH (2018) Isolation and validation of a candidate RSV3 gene from a soybean that confers strain-specific resistance to soybean sosaic virus. Virology 513:153–159

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-SEq. Bioinformatics 25:1105–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456

    Article  PubMed  Google Scholar 

  • Wang BJ, Zhang ZG, Xg LI, Wang YJ, He CY, Zhang JS, Chen SY (2003a) Cloning and analysis of a disease resistance gene homolog from soybean. Acta Botan Sin 45:864–870

    CAS  Google Scholar 

  • Wang X, Gai J, Pu Z (2003b) Classification and distribution of strain groups of soybean mosaic virus in middle and lower Huang-huai and Changjiang valleys. Soybean Sci 22:102–107

    Google Scholar 

  • Wang D, Ma Y, Yang Y, Liu N, Li C, Song Y (2011) Fine mapping and analyses of r (sc8) resistance candidate genes to soybean mosaic virus in soybean. Theor Appl Genet 122:555–565

    Article  PubMed  Google Scholar 

  • Wang J, Shine MB, Gao QM, Navarre D, Jiang W, Liu C, Chen Q, Hu G, Kachroo A (2014a) Enhanced disease susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiol 165:1269–1284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Khatabi B, Hajimorad MR (2014b) Amino acid substitutionin P3 of Soybean mosaic virus to convert avirulence to virulence on Rsv4-genotype soybean is influenced by the genetic composition of P3. Mol Plant Pathol 16:301–307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Z, Yao L, Singer SD, Muhammad H, Zhi L, Wang X (2017) Constitutive heterologous overexpression of a TIR-NB-ARC-LRR gene encoding a putative disease resistance protein from wild Chinese Vitis pseudoreticulata, in Arabidopsis and tobacco enhances resistance to phytopathogenic fungi and bacteria. Plant Physiol Biochem 112:346–361

    Article  CAS  PubMed  Google Scholar 

  • Whitham S, Dineshkumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 114:1101–1115

    Article  Google Scholar 

  • Whitham SA, Qi M, Innes RW, Ma W, Lopes-Caitar V, Hewezi T (2016) Molecular soybean-pathogen interactions. Annu Rev Phytopathol 54:443–468

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Li Y, Yan Y, Wang K, Gao Y, Hu Y (2010) Genome-scale identification of soybean BURP domain-containing genes and their expression under stress treatments. BMC Plant Biol 10:197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  CAS  PubMed  Google Scholar 

  • Yan H, Wang H, Cheng H, Hu Z, Chu S, Zhang G, Yu D (2015) Detection and fine-mapping of sc7 resistance genes via linkage and association analysis in soybean. J Integr Plant Biol 57:722–729

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Lin J, Zheng G, Zhang M, Zhi H (2014) Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Arch Virol 159:1793–1796

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Li B, Zheng X, Li J, Yang M, Dong X, He G, An C, Deng XW (2015a) Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids. Nat Commun 6:7309

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Ling X, Chen T, Cai L, Liu T, Wang J (2015b) A cotton gbvdr5, gene encoding a leucine-rich-repeat receptor-like protein confers resistance to verticillium dahliae, in transgenic Arabidopsis, and upland cotton. Plant Mol Biol Rep 33:987–1001

    Article  CAS  Google Scholar 

  • Yang X, Niu L, Zhang W, He H, Yang J, Xing G, Guo D, Du Q, Qian X, Yao Y, Li Q, Dong Y (2017) Robust RNAi-mediated resistance to infection of seven potyvirids in soybean expressing an intron hairpin NIb RNA. Transgenic Res 26:665–676

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Niu L, Zhang W, Yang J, Xing G, He H, Guo D, Du Q, Qian X, Yao Y, Li Q, Dong Y (2018) RNAi-mediated SMV P3 cistron silencing confers significantly enhanced resistance to multiple Potyvirus strains and isolates in transgenic soybean. Plant Cell Rep 37:103–114

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    Article  CAS  PubMed  Google Scholar 

  • Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omics J Integr Biol 16:284–287

    Article  CAS  Google Scholar 

  • Yue JX, Meyers BC, Chen JQ, Tian D, Yang S (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Grosic S, Whitham SA, Hill JH (2012a) The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to soybean mosaic virus. Mol Plant Microbe Interact 25:1307–1313

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Cui X, Chen X, Zhi H, Zhang S, Zhao L (2012b) Determination of the complete genomic sequence and molecular biological analysiso f soybean mosaic virus. Can J Plant Pathol 34:288–297

    Article  CAS  Google Scholar 

  • Zheng HQ, Zhang Q, Li HX, Lin SZ, An XM, Zhang ZY (2011) Over-expression of the triploid white poplar ptdrl01 gene in tobacco enhances resistance to tobacco mosaic virus. Plant Biol 13:145–153

    Article  CAS  PubMed  Google Scholar 

  • Zhi H, Gai J, He X (2005) Study on methods of classification of quantitative resistance to soybean mosaic virus in soybean. Soybean Sci 22:102–107

    Google Scholar 

  • Zhou GC, Wu XY, Zhang YM, Wu P, Wu XZ, Liu LW, Wang Q, Hang YY, Yang JY, Shao ZQ (2014a) A genomic survey of thirty soybean-infecting bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Res 191:125–133

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, He H, Liu R, Han Q, Shou H, Liu B (2014b) Overexpression of GmAKT2 potassium channel enhances resistance to soybean mosaic virus. BMC Plant Biol 14:154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou GC, Shao ZQ, Ma FF, Wu P, Wu XY, Xie ZY, Yu DY, Cheng H, Liu ZH, Jiang ZF, Chen QS, Wang B, Chen JQ (2015) The evolution of soybean mosaic virus: an updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res 208:189–198

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Haijian Zhi (Nanjing Agricultural University) for providing the virus strains. This work was supported by the National Key R&D Program of China (2016YFD0101902), the China National Novel Transgenic Organisms Breeding Project (2016ZX08004-004) and the Programme for Introducing Talents to Universities (B07017). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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BL, SW, XF, YD and JP designed the research. HX, XY, HH, MW, PG and YW performed the experiments, HX, XY, JP and BL analyzed the data, HX and SW drafted the manuscript, and all authors participated in the revision of the manuscript.

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Correspondence to Jinsong Pang, Yingshan Dong or Shucai Wang.

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Xun, H., Yang, X., He, H. et al. Over-expression of GmKR3, a TIR–NBS–LRR type R gene, confers resistance to multiple viruses in soybean. Plant Mol Biol 99, 95–111 (2019). https://doi.org/10.1007/s11103-018-0804-z

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