SEARCHNARRATIVE_REVIEWplant pathology, agriculture

narrative_review·plant pathology, agriculture, genetics, biotechnology·PMC10204772

Major viral diseases in grain legumes: designing disease resistant legumes from plant breeding and OMICS integration

Frontiers in Plant Science · 11 authors, 11 centres

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This review summarizes major viral diseases affecting grain legumes (soybean, common bean, cowpea, chickpea, mungbean, urdbean, pigeonpea, groundnut) and their significant yield losses, which can reach up to 100%. It describes the genetic resources, QTL mapping, GWAS, functional genomics, and genetic engineering (RNAi, CRISPR) approaches used to develop virus-resistant legume cultivars. The clinical significance lies in ensuring food security by reducing crop losses through sustainable, eco-friendly disease management strategies.

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**Background** Grain legumes are essential for human nutrition and agroecosystems, but viral diseases cause severe yield losses globally, estimated at $30 billion annually and up to 50% of plant diseases. Climate change exacerbates the incidence of these diseases. This review covers major viral pathogens in key grain legumes, including soybean mosaic virus (SMV), bean common mosaic virus (BCMV), mungbean yellow mosaic virus (MYMV), pigeonpea sterility mosaic virus (PPSMV), and others. It discusses the genetic basis of resistance, molecular mechanisms (PTI/ETI), and the integration of omics and breeding technologies to develop resistant cultivars.

**Methods** The authors conducted a narrative review of published literature on viral diseases in grain legumes, focusing on resistance sources, genetics, QTL mapping, genome-wide association studies (GWAS), transcriptomics, and genetic engineering approaches (RNAi, CRISPR/Cas9). They compiled data from multiple studies on biparental QTL mapping, GWAS, and functional genomics in soybean, common bean, cowpea, mungbean, urdbean, pigeonpea, and groundnut. The review also covers emerging breeding tools like genomic selection, rapid generation advancement, and synthetic biology.

**Key Results** - **Soybean**: SMV resistance is controlled by multiple genes (Rsv1, Rsv3, Rsv4, Rsv5) mapped to chromosomes 13, 14, 2, and others. QTLs for SMV resistance explain up to 71-76% phenotypic variation (e.g., qSMV13). GWAS identified loci for TRSV sensitivity on chromosome 2. RNAi targeting HC-Pro or replicase genes conferred resistance to multiple potyviruses. CRISPR/Cas9 editing of GmF3H1, GmF3H2, and GmFNSII-1 increased isoflavone content and SMV resistance. - **Common bean**: BCMV resistance is governed by dominant I gene and recessive bc-1, bc-2, bc-3 genes. BGYMV resistance is controlled by bgm-1 and bgm-2. GWAS mapped BCMNV resistance to PV03 and PV05 chromosomes. RNAi silencing of AC1 gene conferred resistance to BGMV. - **Cowpea**: CPSMV and CABMV cause 13-87% yield losses. RNAi targeting proteinase cofactor and coat protein provided resistance. Exogenous dsRNA application reduced BCMV and GBNV infection. - **Mungbean/Urdbean**: MYMV/MYMIV cause up to 100% yield losses. QTLs on chromosomes 4, 6, 9, and 10 explain 6.2-70% phenotypic variation. Recessive digenic inheritance reported. CRISPR/Cas9 targeting AC1 and AV1 genes of MYMV was attempted. - **Pigeonpea**: PPSMV causes >US$300 million losses annually in India. QTLs on LG2, LG3, LG7, LG10, LG11 explain 5.2-34.3% phenotypic variation. Resistance sources include wild relatives (C. albicans, C. platycarpus). - **Groundnut**: PBNV causes 30-90% yield losses. QTLs for TSWV resistance on A01, A04, A09, B02, B04, B10 explain 7-37% phenotypic variation. - **Chickpea**: CSD causes up to 95% yield loss. CMV incidence of 75% leads to 45% yield loss. Resistance sources include wild Cicer species.

**Clinical Implications** Developing virus-resistant grain legumes is critical for sustainable food production and combating malnutrition. The integration of genomics, transcriptomics, and genetic engineering (RNAi, CRISPR) with advanced breeding (genomic selection, speed breeding) can accelerate the development of resistant cultivars. However, challenges include virus evolution, off-target effects, transformation recalcitrance, and regulatory hurdles for genome-edited plants. Continued research is needed to ensure durable resistance and address co-infections.

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narrative_review

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plant pathology

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ORIGINAL PAPER

PMC10204772

Major viral diseases in grain legumes: designing disease resistant legumes from plant breeding and OMICS integration

Frontiers in Plant Science

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ABSTRACT

Abstract Grain legumes play a crucial role in human nutrition and as a staple crop for low-income farmers in developing and underdeveloped nations, contributing to overall food security and agroecosystem services. Viral diseases are major biotic stresses that severely challenge global grain legume production. In this review, we discuss how exploring naturally resistant grain legume genotypes within germplasm, landraces, and crop wild relatives could be used as promising, economically viable, and eco-environmentally friendly solution to reduce yield losses. Studies based on Mendelian and classical genetics have enhanced our understanding of key genetic determinants that govern resistance to various viral diseases in grain legumes. Recent advances in molecular marker technology and genomic resources have enabled us to identify genomic regions controlling viral disease resistance in various grain legumes using techniques such as QTL mapping, genome-wide association studies, whole-genome resequencing, pangenome and ‘omics’ approaches. These comprehensive genomic resources have expedited the adoption of genomics-assisted breeding for developing virus-resistant grain legumes. Concurrently, progress in functional genomics, especially transcriptomics, has helped unravel underlying candidate gene(s) and their roles in viral disease resistance in legumes. This review also examines the progress in genetic engineering-based strategies, including RNA interference, and the potential of synthetic biology techniques, such as synthetic promoters and synthetic transcription factors, for creating viral-resistant grain legumes. It also elaborates on the prospects and limitations of cutting-edge breeding technologies and emerging biotechnological tools (e.g., genomic selection, rapid generation advances, and CRISPR/Cas9-based genome editing tool) in developing virus-disease-resistant grain legumes to ensure global food security. Keywords: Grain legume, disease, virus, QTL, genome sequence, PTI, ETI

CITATION EXPORT

Uday Chand Jha, Harsh Nayyar, Anirudha Chattopadhyay et al.. Major viral diseases in grain legumes: designing disease resistant legumes from plant breeding and OMICS integration. Frontiers in Plant Science. (2023). https://doi.org/10.3389/fpls.2023.1183505

AUTHORS

11 · 11 CENTRES

Uday Chand Jha, Harsh Nayyar, Anirudha Chattopadhyay, Radha Beena, Ajaz A Lone, Yogesh Dashrath Naik, Mahendar Thudi, Pagadala Venkata Vara Prasad, Sanjeev Gupta, Girish Prasad Dixit, Kadambot H M Siddique

1 Indian Institute of Pulses Research (IIPR), Indian Council of Agricultural Research (ICAR), Kanpur, Uttar Pradesh, India
2 Department of Botany, Panjab University, Chandigarh, India
3 Department of Plant Pathology, Pulse Research Station, S.D. Agricultural University SK Nagar, SK Nagar, Gujarat, India
4 Department of Plant Physiology, College of Agriculture, Vellayani, Kerala Agricultural University (KAU), Thiruvananthapuram, Kerala, India
5 Dryland Agriculture Research Station, Sher-e-Kashmir University of Agricultural Sciences and Technology (SKUAST)-Kashmir, Srinagar, India
6 Department of Agricultural Biotechnology and Molecular Biology, Dr. Rajendra Prasad Central Agricultural University, Samatipur, Bihar, India
7 Shandong Academy of Agricultural Sciences, Jinan, Shandong, China
8 Center for Crop Health, University of Southern Queensland, Toowoomba, QLD, Australia
9 Department of Agronomy, Kansas State University, Manhattan, KS, United States
10 Indian Council of Agricultural Research, New Delhi, India
11 The University of Western Australia (UWA) Institute of Agriculture, The University of Western Australia, Perth, WA, Australia