qMrdd3, a major QTL conferring durable resistance to maize rough dwarf disease

doi:10.1016/j.jia.2025.07.004

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qMrdd3, a major QTL conferring durable resistance to maize rough dwarf disease

Qingkang Wang¹^*, Weixiao Zhang²^*, Suining Deng²*, Fei Ni¹, Wei Xu¹, Qingzhi Liu¹, Yuqiang Diao¹, Yongzhong Zhang¹, Mingliang Xu²^#, Baoshen Liu¹^#

¹College of Agronomy, Shandong Agricultural University, Tai’an 271018, China

² State Key Laboratory of Maize Bio-breeding, Frontiers Science Center for Molecular Design Breeding/Joint International Research Laboratory of Crop Molecular Breeding, National Maize Improvement Center/College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China

Highlights

The major QTL-qMrdd3 on chromosome 2 explained 12.71% of the total phenotypic variations and reduced DSI by 26.36–34.47% across multiple environments.

Fine-mapping delimited qMrdd3 to a 227.7-kb region containing five genes, including Zm00001d002441, which was significantly upregulated in the resistant line NIL-R after RBSDV infection.

Two co-segregating markers enabled efficient introgression of qMrdd3 into susceptible lines Zheng58 and Chang 7-2, reducing DSI by 26.47–38.84%, highlighting its potential for accelerating MRDD-resistant breeding.

Abstract
References

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摘要

玉米粗缩病（Maize rough dwarf disease, MRDD）是由斐济病毒属病毒（Fijivirus）引起的病毒性病害，对全球玉米生产构成重大威胁。我们利用抗病亲本CML199和感病亲本郑58构建的重组自交系（Recombinant inbred line, RIL）群体，鉴定到了三个玉米粗缩病抗性数量性状基因座（Quantitative trait loci, QTLs）分别在第2、6和9号染色体上，解释了12.71%、5.89%和11.04%的表型变异。其中，位于第2号染色体上的主效基因座qMrdd3表现为不完全显性，在不同环境下能提高26.36–34.47%的抗性。通过精细定位，我们将qMrdd3限定在227.7 kb的区间内，该区间包含5个候选基因。其中，病毒（水稻黑条矮缩病毒，Rice black-streaked dwarf virus, RBSDV）侵染抗病近等基因系（Resistant near-isogenic line, NIL-R）后，Zm00001d002441 特异性上调表达。此外，我们还开发了两个共分离标记，用于高效的标记辅助选择。将qMrdd3导入感病自交系郑58和昌7-2后，抗性分别提高了38.84%和26.47%。本研究通过QTL解析、优良种质创制和标记辅助育种，为玉米粗缩病抗性育种提供了宝贵的遗传资源。

Abstract

Maize rough dwarf disease (MRDD), caused by Fijivirus, poses a significant threat to global maize production. Using a recombinant inbred line (RIL) population derived from the resistant parent CML199 and the susceptible parent Zheng58, we identified three MRDD resistance QTLs on chromosomes 2, 6, and 9, accounting for 12.71, 5.89, and 11.04% of the total phenotypic variation, respectively. Among them, the major locus qMrdd3 on chromosome 2 demonstrated incomplete dominance, conferring a resistance enhancement of 26.36–34.47% across diverse environments. Fine-mapping refined qMrdd3 to a 227.7-kb interval containing five candidate genes, among which Zm00001d002441 was specifically upregulated in the resistant near-isogenic line (NIL-R) following RBSDV infection. Additionally, two co-segregating markers were developed to facilitate efficient marker-assisted selection. Introgression of qMrdd3 into Zheng58 and Chang7-2 enhanced field resistance by 38.84 and 26.47%, respectively. This study provides a valuable genetic resource for MRDD resistance breeding through QTL dissection, elite germplasm development, and marker-assisted breeding.

Keywords: Zea mays MRDD QTL Fine-mapping MAS

Online: 05 July 2025

Fund:

This work was funded by the Key R&D Program of Shandong Province (2022LZGC006 and 2022LZGCQY017), the Natural Science Foundation of China (31971950), and the Innovative Technology Guidance Program of Shandong, China (Central Government Guides Local Science and Technology Development Funds) (YDZX2023063).

About author: #Correspondence Mingliang Xu, Tel: +86-10-62733166, E-mail: mxu@cau.edu.cn; Baoshen Liu, Tel: +86-538-8242226, E-mail: liubs@sdau.edu.cn * These authors contributed equally to this study.

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Qingkang Wang, Weixiao Zhang, Suining Deng, Fei Ni, Wei Xu, Qingzhi Liu, Yuqiang Diao, Yongzhong Zhang, Mingliang Xu, Baoshen Liu. 2025. qMrdd3, a major QTL conferring durable resistance to maize rough dwarf disease. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.07.004

Abendroth L J, Elmore R W, Boyer M J, Marlay S K. 2011. Corn Growth and Development. Iowa State University, Ames, Iowa.

Arneodo J D, Guzmán F A, Conci L R, Laguna I G, Truol G. 2002. Transmission features of Mai de Río Cuarto virus in wheat by its planthopper vector Delphacodes kuscheli. Annals of Applied Biology, 141, 195–200.

Bai F W, Yan J, Qu Z C, Zhang H W, Xu J, Ye M M, Shen D L. 2002. Phylogenetic analysis reveals that a dwarfing disease on different cereal crops in China is due to rice black streaked dwarf virus (RBSDV). Virus Genes, 25, 201–206.

Broman K W, Wu H, Sen Ś, Churchill G A. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics, 19, 889–890.

Caciagli P, Casetta A. 1986. Maize rough dwarf virus (Reoviridae) in its planthopper vector Laodelphax striatellus in relation to vector infectivity. Annals of Applied Biology, 109, 337–344.

Chen G, Zhang B, Ding J, Wang H, Deng C, Wang J, Yang Q, Pi Q, Zhang R, Zhai H, Dong J, Huang J, Hou J, Wu J, Que J, Zhang F, Li W, Min H, Tabor G, Li B, Liu X, Zhao J, Yan J, Lai Z. 2022. Cloning southern corn rust resistant gene RppK and its cognate gene AvrRppK from Puccinia polysora. Nature Communications, 13, 4392.

Cheng Z, Li S, Gao R, Sun F, Liu W, Zhou J, Wu J, Zhou X, Zhou Y. 2013. Distribution and genetic diversity of Southern rice black-streaked dwarf virus in China. Virology Journal, 10, 307.

Collins C A, LaMontagne E D, Anderson J, Ekanayake G, Clarke A S, Bond L N, Salamango D J, Cornish P V, Peck S C, Heese A. 2020. EPSIN1 modulates the plasma membrane abundance of FLAGELLIN SENSING2 for effective immune responses. Plant Physiology, 182, 1762–1775.

Deng S, Jiang S, Liu B, Zhong T, Liu Q, Liu J, Liu Y, Yin C, Sun C, Xu M. 2024. ZmGDIα-hel counters the RBSDV-induced reduction of active gibberellins to alleviate maize rough dwarf virus disease. Nature Communications, 15, 7576.

Dovas C I, Eythymiou K, Katis N I. 2004. First report of Maize rough dwarf virus (MRDV) on maize crops in Greece. Plant Physiology, 53, 238–238.

Fang S, Yu J, Feng J, Han C, Li D, Liu Y. 2001. Identification of rice black-streaked dwarf fijivirus in maize with rough dwarf disease in China. Archives of Virology, 146, 167–170.

Huang Q, Li W, Wang Z, He K. 2011. Research situation and prospect of maize rough dwarf disease. Journal of Maize Sciences, 19, 140–143.

Huth W, Maurath R, Imgraben H, Schröder M. 2007. Maize rough dwarf virus for the first time detected in Germany. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 59, 173–175.

Kang B C, Yeam I, Jahn M M. 2005. Genetics of plant virus resistance. Annual Review of Phytopathology, 43, 581–621.

Lenardon S L, March G J, Nome S F, Ornaghi J A. 1998. Recent outbreak of “Mal de Río Cuarto” virus on corn in Argentina. Plant Disease, 82, 448.

Li G, Xu Z, Wang J, Mu C, Zhou Z, Li M, Hao Z, Zhang D, Yong H, Han J, Li X, Zhao J, Weng J. 2024. Gene pyramiding of ZmGLK36 and ZmGDIα-hel for rough dwarf disease resistance in maize. Molecular Breeding, 44, 25.

Li R, Song W, Wang B, Wang J, Zhang D, Zhang Q, Li X, Wei J, Gao Z. 2018. Identification of a locus conferring dominant resistance to maize rough dwarf disease in maize. Scientific Reports, 8, 3248.

Li Y, Tao X, Yao L, Tang S, Zhang X, Tong L, Liu Q, Song T, Zhang D, Cao Y, Zhong T, Xu M. 2025. qRfv2, a quantitative resistance locus against Fusarium ear rot in maize. The Crop Journal, 13, 41–50.

Liu C, Hua J, Liu C, Zhang D, Hao Z, Yong H, Xie C, Li M, Zhang S, Weng J, Li X. 2016. Fine mapping of a quantitative trait locus conferring resistance to maize rough dwarf disease. Theoretical and Applied Genetics, 129, 2333–2342.

Liu Q, Deng S, Liu B, Tao Y, Ai H, Liu J, Zhang Y, Zhao Y, Xu, M. 2020. A helitron-induced RabGDIα variant causes quantitative recessive resistance to maize rough dwarf disease. Nature Communications, 11, 495.

Luan J, Wang F, Li Y, Zhang B, Zhang J. 2012. Mapping quantitative trait loci conferring resistance to rice black-streaked virus in maize (Zea mays L.). Theoretical and Applied Genetics, 125, 781–791.

Lv X, Song M, Cheng Z, Yang X, Zhang X, Zhou Z, Zhang C, Zheng L, Li Y, Lei K, Wang H, Du W, Li F, Li X, Weng J. 2020. qGLS1.02, a novel major locus for resistance to gray leaf spot in maize. Molecular Breeding, 40, 59.

Milne R G, Lovisolo O. 1977. Maize rough dwarf and related viruses. Advances in Virus Research, 21, 267–341.

Di Renzo M A, Bonamico N C, Díaz D D, Salerno J C, Ibañez M M, Gesumaria J J. 2002. Inheritance of resistance to Mal de Río Cuarto (MRC) disease in Zea mays (L.). The Journal of Agricultural Science, 139, 47–53.

Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.

Shi L, Weng J, Liu C, Song X, Miao H, Hao Z, Xie C, Li M, Zhang D, Bai L, Pan G, Li X, Zhang S. 2013. Identification of promoter motifs regulating ZmeIF4E expression level involved in maize rough dwarf disease resistance in maize (Zea mays L.). Molecular Genetics and Genomics, 288, 89–99.

Soosaar J L, Burch-Smith T M, Dinesh-Kumar S P. 2005. Mechanisms of plant resistance to viruses. Nature Reviews Microbiology, 3, 789–798.

Tao Y, Liu Q, Wang H, Zhang Y, Huang X, Wang B, Lai J, Ye J, Liu B, Xu M. 2013. Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease. BMC Plant Biology, 13, 145.

Wang B, Hou M, Shi J, Ku L, Song W, Li C, Ning Q, Li X, Li C, Zhao B, Zhang R, Xu H, Bai Z, Xia Z, Wang H, Kong D, Wei H, Jing Y, Dai Z, Wang H H, et al. 2023. De novo genome assembly and analyses of 12 founder inbred lines provide insights into maize heterosis. Nature Genetics, 55, 312–323.

Wang R, Du K, Jiang T, Di D, Fan Z, Zhou T. 2022. Comparative proteomic analyses of susceptible and resistant maize inbred lines at the stage of enations forming following infection by rice black-streaked dwarf virus. Viruses, 14, 2604.

Wang X, Yang Q, Dai Z, Wang Y, Zhang Y, Li B, Zhao W, Hao J. 2019. Identification of QTLs for resistance to maize rough dwarf disease using two connected RIL populations in maize. PLoS ONE, 14, e0226700.

Xu L, Zhang Y, Shao S, Chen W, Tan J, Zhu M, Zhong T, Fan X, Xu M. 2014. High-resolution mapping and characterization of qRgls2, a major quantitative trait locus involved in maize resistance to gray leaf spot. BMC Plant Biology, 14, 230.

Xu Z, Hua J, Wang F, Cheng Z, Meng Q, Chen Y, Han X, Tie S, Liu C, Li X, Wang Z, Weng J. 2020. Marker-assisted selection of qMrdd8 to improve maize resistance to rough dwarf disease. Breeding Science, 70, 183–192.

Xu Z, Wang F, Zhou Z, Meng Q, Chen Y, Han X, Tie S, Liu C, Hao Z, Li M, Zhang D, Han J, Wang Z, Li X, Weng J. 2022. Identification and fine-mapping of a novel QTL, qMrdd2, that confers resistance to maize rough dwarf disease. Plant Disease, 106, 65–72.

Xu Z, Zhou Z, Cheng Z, Zhou Y, Wang F, Li M, Li G, Li W, Du Q, Wang K, Lu X, Tai Y, Chen R, Hao Z, Han J, Chen Y, Meng Q, Kong X, Tie S, Mu C, et al. 2023. A transcription factor ZmGLK36 confers broad resistance to maize rough dwarf disease in cereal crops. Nature Plants, 9, 1720–1733.

Yang Q, Balint-Kurti P, Xu M. 2017. Quantitative disease resistance: Dissection and adoption in maize. Molecular Plant, 10, 402–413.

Yang Q, Zhang D, Xu M. 2012. A sequential quantitative trait locus fine-mapping strategy using recombinant-derived progeny. Journal of Integrative Plant Biology, 54, 228–237.

Yang Y, Wang A, Wang M, Zhang Y, Zhang J, Zhao M. 2022. ATP-binding cassette transporters ABCF2 and ABCG9 regulate rice black-streaked dwarf virus infection in its insect vector, Laodelphax striatellus (Fallén). Bulletin of Entomological Research, 112, 327–334.

Yin X, Xu F F, Zheng F Q, Li X D, Liu B S, Zhang C Q. 2011. Molecular characterization of segments S7 to S10 of a southern rice black-streaked dwarf virus isolate from maize in northern China. Virologica Sinica, 26, 47–53.

Yue R, Sun Q, Ding J, Li W, Li W, Zhao M, Lu S, Zeng T, Zhang H, Zhao S, Tie S, Meng Z. 2022. Functional analysis revealed the involvement of ZmABCB15 in resistance to rice black-streaked dwarf virus infection. BMC Plant Biology, 22, 484.

Zhang H, Chen J, Lei J, Adams M J. 2001. Sequence analysis shows that a dwarfing disease on rice, wheat and maize in China is caused by rice black-streaked dwarf virus. European Journal of Plant Pathology, 107, 563–567.

Zhang J, Dong Y, Wang M, Wang H, Yi D, Zhou Y, Xu Q. 2021. MicroRNA-315-5p promotes rice black-streaked dwarf virus infection by targeting a melatonin receptor in the small brown planthopper. Pest Management Science, 77, 3561–3570.

Zhang W, Deng S, Zhao Y, Xu W, Liu Q, Zhang Y, Ren C, Cheng Z, Xu M, Liu B. 2021. qMrdd2, a novel quantitative resistance locus for maize rough dwarf disease. BMC Plant Biology, 21, 307.

Zhao M, Liu S, Pei Y, Jiang X, Jaqueth J S, Li B, Han J, Jeffers D, Wang J, Song X. 2022. Identification of genetic loci associated with rough dwarf disease resistance in maize by integrating GWAS and linkage mapping. Plant Science, 315, 111100.

Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, Xing Y, Zhang B, Liu H, Fengler K A, Zhao J, Zhao X, Chen Y, Lai J, Yan J, Xu M. 2015. A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 47, 151–157.

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