Unraveling the genetics of heat tolerance in chickpea landraces (Cicer arietinum L.) using genome-wide association studies

Thippeswamy Danakumara; Neeraj Kumar; Basavanagouda Siddanagouda Patil; Tapan Kumar; Chellapilla Bharadwaj; Pradeep Kumar Jain; Manduparambil Subramanian Nimmy; Nilesh Joshi; Swarup Kumar Parida; Shayla Bindra; Chittaranjan Kole; Rajeev K Varshney

doi:10.3389/fpls.2024.1376381

Unraveling the genetics of heat tolerance in chickpea landraces (Cicer arietinum L.) using genome-wide association studies

Front Plant Sci. 2024 Mar 25:15:1376381. doi: 10.3389/fpls.2024.1376381. eCollection 2024.

Affiliations

¹ ICAR- Indian Agricultural Research Institute, New Delhi, India.
² International Centre for Agricultural Research in the Dry Areas, Amlaha, Madhya Pradesh, India.
³ ICAR-National Institute for Plant Biotechnology, New Delhi, India.
⁴ National Institute of Plant Genome Research (NIPGR), New Delhi, India.
⁵ Punjab Agricultural University, Ludhiana, India.
⁶ Prof. Chittaranjan Kole Foundation for Science & Society, Kolkatta, India.
⁷ Murdoch University, Murdoch, WA, Australia.

Abstract

Chickpea, being an important grain legume crop, is often confronted with the adverse effects of high temperatures at the reproductive stage of crop growth, drastically affecting yield and overall productivity. The current study deals with an extensive evaluation of chickpea genotypes, focusing on the traits associated with yield and their response to heat stress. Notably, we observed significant variations for these traits under both normal and high-temperature conditions, forming a robust basis for genetic research and breeding initiatives. Furthermore, the study revealed that yield-related traits exhibited high heritability, suggesting their potential suitability for marker-assisted selection. We carried out single-nucleotide polymorphism (SNP) genotyping using the genotyping-by-sequencing (GBS) method for a genome-wide association study (GWAS). Overall, 27 marker-trait associations (MTAs) linked to yield-related traits, among which we identified five common MTAs displaying pleiotropic effects after applying a stringent Bonferroni-corrected p-value threshold of <0.05 [-log₁₀(p) > 4.95] using the BLINK (Bayesian-information and linkage-disequilibrium iteratively nested keyway) model. Through an in-depth in silico analysis of these markers against the CDC Frontier v1 reference genome, we discovered that the majority of the SNPs were located at or in proximity to gene-coding regions. We further explored candidate genes situated near these MTAs, shedding light on the molecular mechanisms governing heat stress tolerance and yield enhancement in chickpeas such as indole-3-acetic acid-amido synthetase GH3.1 with GH3 auxin-responsive promoter and pentatricopeptide repeat-containing protein, etc. The harvest index (HI) trait was associated with marker Ca3:37444451 encoding aspartic proteinase ortholog sequence of Oryza sativa subsp. japonica and Medicago truncatula, which is known for contributing to heat stress tolerance. These identified MTAs and associated candidate genes may serve as valuable assets for breeding programs dedicated to tailoring chickpea varieties resilient to heat stress and climate change.

Keywords: QTN; chickpea; genome-wide association study (GWAS); heat; single-nucleotide polymorphism (SNPs).

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Part of the research was supported by a grant from the Bill and Melinda Gates Foundation to ICAR-IARI for chickpea (grant number #OPP1194767) and partly from the CRP Molecular Breeding Project of ICAR. Funding was provided by PG School to the first author and by ICAR-IARI for research and field facilities to the senior authors.