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Genetic networks underlying salinity tolerance in wheat uncovered with genome-wide analyses and selective sweeps

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Abstract

Key Message

A genetic framework underpinning salinity tolerance at reproductive stage was revealed by genome-wide SNP markers and major adaptability genes in synthetic-derived wheats, and trait-associated loci were used to predict phenotypes.

Abstract

Using wild relatives of crops to identify genes related to improved productivity and resilience to climate extremes is a prioritized area of crop genetic improvement. High salinity is a widespread crop production constraint, and development of salt-tolerant cultivars is a sustainable solution. We evaluated a panel of 294 wheat accessions comprising synthetic-derived wheat lines (SYN-DERs) and modern bread wheat advanced lines under control and high salinity conditions at two locations. The GWAS analysis revealed a quantitative genetic framework of more than 200 loci with minor effect underlying salinity tolerance at reproductive stage. The significant trait-associated SNPs were used to predict phenotypes using a GBLUP model, and the prediction accuracy (r2) ranged between 0.57 and 0.74. The r2 values for flag leaf weight, days to flowering, biomass, and number of spikes per plant were all above 0.70, validating the phenotypic effects of the loci discovered in this study. Furthermore, the germplasm sets were compared to identify selection sweeps associated with salt tolerance loci in SYN-DERs. Six loci associated with salinity tolerance were found to be differentially selected in the SYN-DERs (12.4 Mb on chromosome (chr)1B, 7.1 Mb on chr2A, 11.2 Mb on chr2D, 200 Mb on chr3D, 600 Mb on chr6B, and 700.9 Mb on chr7B). A total of 228 reported markers and genes, including 17 well-characterized genes, were uncovered using GWAS and EigenGWAS. A linkage disequilibrium (LD) block on chr5A, including the Vrn-A1 gene at 575 Mb and its homeologs on chr5D, were strongly associated with multiple yield-related traits and flowering time under salinity stress conditions. The diversity panel was screened with more than 68 kompetitive allele-specific PCR (KASP) markers of functional genes in wheat, and the pleiotropic effects of superior alleles of Rht-1, TaGASR-A1, and TaCwi-A1 were revealed under salinity stress. To effectively utilize the extensive genetic information obtained from the GWAS analysis, a genetic interaction network was constructed to reveal correlations among the investigated traits. The genetic network data combined with GWAS, selective sweeps, and the functional gene survey provided a quantitative genetic framework for identifying differentially retained loci associated with salinity tolerance in wheat.

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All the phenotypic is available as supplementary material, and genotypic data will be made available on the reasonable request to corresponding author.

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Funding

This work was funded by the National Science Foundation of China (32022064), and the Project of Hainan Yazhou Bay Seed Lab (B21HJ0223).

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Author notes

  1. Danting Shan and Mohsin Ali have contributed to the work equally.

Authors and Affiliations

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), CIMMYT-China Office, 12 Zhongguancun South Street, Beijing, 100081, China

    Danting Shan, Mohsin Ali, Xianchun Xia, Awais Rasheed, Zhonghu He & Huihui Li

  2. Nanfan Research Institute, CAAS, Sanya, 572024, Hainan, China

    Danting Shan, Mohsin Ali & Huihui Li

  3. International Center for Biosaline Agriculture (ICBA), Al Ruwayyah 2, Academic City, Dubai, UAE

    Mohammed Shahid

  4. National Institute of Agriculture and Biology (NIAB), Faisalabad, Pakistan

    Anjuman Arif & Muhammad Qandeel Waheed

  5. Plant Breeding Institute, School of Life and Environmental Sciences, The University of Sydney, Sydney, 2006, Australia

    Richard Trethowan

  6. Division of Biological and Environmental Sciences and Engineering (BESE), King Abdullah University of Science and Technology (KASUT), Thuwal, 23955-6900, Saudi Arabia

    Mark Tester & Jesse Poland

  7. Kansas State University, Manhattan, KS, USA

    Jesse Poland

  8. Grains Research and Development Corporation (GRDC), Kingston, Australia

    Francis C. Ogbonnaya

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  1. Danting Shan
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  2. Mohsin Ali
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Contributions

HL, AR, and ZH conceived and designed the study; DS, HL, and AR analyzed the data and wrote the manuscript; AR and XX generated KASP marker data; MT performed the salinity experiments; JP generated GBS data; MA, MS, AA, and MQW performed field experiments at Pakistan; MA, RT, FCO, JP, MT, and ZH edited the manuscript. All authors have read and approved the manuscript.

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Correspondence to Awais Rasheed or Huihui Li.

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Shan, D., Ali, M., Shahid, M. et al. Genetic networks underlying salinity tolerance in wheat uncovered with genome-wide analyses and selective sweeps. Theor Appl Genet 135, 2925–2941 (2022). https://doi.org/10.1007/s00122-022-04153-5

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