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An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize Qingqing Liu China Agricultural University

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An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize Qingqing Liu China Agricultural University Agronomy Publications Agronomy 3-6-2017 An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize Qingqing Liu China Agricultural University Huanhuan Liu China Agricultural University Yangqing Gong China Agricultural University Yongfu Tao China Agricultural University Lu Jiang China Agricultural University See next page for additional authors Follow this and additional works at: https://lib.dr.iastate.edu/agron_pubs Part of the Agronomy and Crop Sciences Commons The ompc lete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ agron_pubs/351. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Agronomy at Iowa State University Digital Repository. It has been accepted for inclusion in Agronomy Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize Abstract Sugarcane mosaic virus (SCMV) causes substantial losses of grain yield and forage biomass in susceptible maize worldwide. A major quantitative trait locus, Scmv1, has been identified to impart strong resistance to SCMV at the early infection stage. Here, we demonstrate that ZmTrxh, encoding an atypical h-type thioredoxin, is the causal gene at Scmv1, and that its transcript abundance correlated strongly with maize resistance to SCMV. ZmTrxh alleles, whether they are resistant or susceptible, share the identical coding/ proximal promoter regions, but vary in the upstream regulatory regions. ZmTrxh lacks two canonical cysteines in the thioredoxin active-site motif and exists uniquely in the maize genome. Because of this, ZmTrxh is unable to reduce disulfide bridges but possesses a strong molecular chaperone-like activity. ZmTrxh is dispersed in maize cytoplasm to suppress SCMV viral RNA accumulation. Moreover, ZmTrxh- mediated maize resistance to SCMV showed no obvious correlation with the salicylic acid- and jasmonic acid- related defense signaling pathways. Taken together, our results indicate that ZmTrxh exhibits a distinct defense profile in maize resistance to SCMV, differing from previously characterized dominant or recessive potyvirus resistance genes. Keywords maize, sugarcane mosaic virus, quantitative resistance gene, h-type thioredoxin Disciplines Agronomy and Crop Sciences Comments This is a manuscript published as Liu, Qingqing, Huanhuan Liu, Yangqing Gong, Yongfu Tao, Lu Jiang, Weiliang Zuo, Qin Yang et al. "An atypical thioredoxin imparts early resistance to Sugarcane Mosaic Virus in Maize." Molecular Plant 10, no. 3 (2017): 483-497. doi: 10.1016/j.molp.2017.02.002. Posted with permission. Authors Qingqing Liu, Huanhuan Liu, Yangqing Gong, Yongfu Tao, Lu Jiang, Weiliang Zuo, Qin Yang, Jianrong Ye, Jinsheng Lai, Jianyu Wu, Thomas Lubberstedt, and Mingliang Xu This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/agron_pubs/351 Accepted Manuscript An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize Qingqing Liu, Huanhuan Liu, Yangqing Gong, Yongfu Tao, Lu Jiang, Weiliang Zuo, Qin Yang, Jianrong Ye, Jinsheng Lai, Jianyu Wu, Thomas Lübberstedt, Mingliang Xu PII: S1674-2052(17)30041-2 DOI: 10.1016/j.molp.2017.02.002 Reference: MOLP 430 To appear in: MOLECULAR PLANT Accepted Date: 1 February 2017 Please cite this article as: Liu Q., Liu H., Gong Y., Tao Y., Jiang L., Zuo W., Yang Q., Ye J., Lai J., Wu J., Lübberstedt T., and Xu M. (2017). An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize. Mol. Plant. doi: 10.1016/j.molp.2017.02.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. All studies published in MOLECULAR PLANT are embargoed until 3PM ET of the day they are published as corrected proofs on-line. Studies cannot be publicized as accepted manuscripts or uncorrected proofs. ACCEPTED MANUSCRIPT 1 An Atypical Thioredoxin Imparts Early Resistance 2 to Sugarcane Mosaic Virus in Maize 3 Qingqing Liu 1, Huanhuan Liu 1, Yangqing Gong 1, Yongfu Tao 1, Lu Jiang 1, Weiliang Zuo 1, Qin Yang 1, 4 Jianrong Ye 1, Jinsheng Lai 1, Jianyu Wu 3, Thomas L übberstedt 2, *, Mingliang Xu 1, * 5 1National Maize Improvement Centre of China, China Agricultural University, Beijing 100193, China 6 2Department of Agronomy, Iowa State University, Ames, IA, 50011, USA 7 3College of Agronomy, Synergetic Innovation Center of Henan Grain Crops and National Key 8 Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, 450002, 9 China 10 11 *Correspondence: Mingliang Xu ([email protected]), Thomas Lübberstedt ([email protected]) 12 13 Running Tittle: Resistance to Sugarcane Mosaic Virus in Maize 14 Short Summary: We report the map-based cloningMANUSCRIPT of the gene ZmTrxh , which confers 15 strong early resistance to sugarcane mosaic virus (SCMV) infection in maize. ZmTrxh 16 encodes an atypical h-type thioredoxin, and its transcript abundance correlates strongly 17 with SCMV resistance. ZmTrxh acts as a molecular chaperone to suppress viral RNA 18 accumulation in cytoplasm without eliciting SA- or JA-mediated defense response. ACCEPTED ACCEPTED MANUSCRIPT 19 ABSTRACT 20 Sugarcane mosaic virus (SCMV) disease causes substantial losses of grain yield and 21 forage biomass in susceptible maize worldwide. A major quantitative trait locus, Scmv1 , 22 has been identified to impart strong resistance to SCMV at early infection stage. Here, we 23 demonstrate that ZmTrxh , encoding an atypical h-type thioredoxin, is the causal gene at 24 Scmv1 , and that its transcript abundance correlated strongly with maize resistance to 25 SCMV. ZmTrxh alleles, whether they are resistant or susceptible, share the identical 26 coding/proximal promoter regions, but vary in the upstream regulatory regions. ZmTrxh 27 lacks two canonical cysteines in the thioredoxin active-site motif and exists uniquely in 28 maize genome. Because of this, ZmTrxh is unable to reduce disulfide bridges, but 29 possesses a strong molecular chaperone-like activity. ZmTrxh is dispersed in maize 30 cytoplasm to suppress SCMV viral RNA accumulation. Moreover, ZmTrxh -mediated 31 maize resistance to SCMV showed no obvious correlation with the SA- and JA-related 32 defense signaling pathways. Altogether, ZmTrxhMANUSCRIPT exhibits a distinct defense profile in 33 maize resistance to SCMV, differing from previously characterized dominant or recessive 34 potyvirus resistance genes. 35 36 Key words : maize, sugarcane mosaic virus, quantitative resistance gene, h-type 37 thioredoxin 38 39 INTRODUCTION 40 Maize ( Zea mays L.) is a widely cultivated cereal crop. It serves as livestock feed, staple 41 food, and isACCEPTED an important source for the biofuel industry. Sugarcane mosaic virus 42 (SCMV), a single positive sense-strand RNA virus belonging to the genus Potyvirus and 43 transmitted by aphid vectors, poses a grave threat to global maize production, especially 44 in Europe, Asia, and Africa (Louie and Darrah, 1980; Melchinger et al., 1998; Zhang et 45 al., 2003). Co-infection of SCMV and maize chlorotic mottle virus (MCMV) results in ACCEPTED MANUSCRIPT 46 maize lethal necrosis (MLN), a recent and rapidly emerging threat of maize production in 47 Eastern Africa (Mahuku et al., 2015). Apart from maize, SCMV also infects sorghum, 48 sugarcane, and other Poaceae species (Shukla et al., 1989). SCMV-infected plants 49 typically display chlorosis in emerging leaves and stunted vegetative growth, resulting in 50 reduced biomass and loss of grain yield. While attempts to control aphids have failed to 51 reduce SCMV incidence, deployment of genetically improved resistant maize varieties 52 has provided an efficient, cost-effective, and environmentally friendly measure to control 53 the disease. Two major resistance quantitative trait loci (QTLs), namely Scmv1 and 54 Scmv2 located on maize chromosomes 6S and 3L, were identified in diverse independent 55 mapping populations to confer resistance to SCMV (Xia et al., 1999; Xu et al., 1999; Wu 56 et al., 2007). Scmv1 confers strong early resistance to SCMV, and Scmv2 mainly 57 functions at later infection stages (Xing et al., 2006). No hypersensitive response (HR) 58 has yet been found to be associate with maize resistance to SCMV (Yuan et al., 2003), 59 implying that neither Scmv1 nor Scmv2 is likely to be a typical NBS-LRR 60 (nucleotide-binding site-leucine-rich repeats) resiMANUSCRIPTstance gene which activates HR. 61 Current knowledge related to antiviral immune responses mostly comes from 62 dicotyledonous plants. Plant species employ various strategies to combat viral attack with 63 mostly characterized mechanisms involving 1) the host antiviral RNA silencing 64 machinery, 2) active defense mediated by dominant resistance ( R) genes, and 3) recessive 65 resistance owing to incompatibility between viral factors and host targets. The host RNA 66 silencing machinery targets and processes the virus-derived double-stranded
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