Genetic diversity, disease resistance, and environmental adaptation of Arachis duranensis L.: New insights from landscape genomics

Authors: Massa, Alicia; Sobolev, Victor; Faustinelli, Paola; Tallury, Shyamalrau - Shyam; STALKER, THOMAS - North Carolina State University; Lamb, Marshall; Arias De Ares, Renee

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/27/2024
Publication Date: 4/16/2024
Citation: Massa, A.N., Sobolev, V., Faustinelli, P.C., Tallury, S.P., Stalker, T., Lamb, M.C., Arias De Ares, R.S. 2024. Genetic diversity, disease resistance, and environmental adaptation of Arachis duranensis L.: New insights from landscape genomics. PLOS ONE. 19(4): e0299992. https://doi.org/10.1371/journal.pone.0299992.
DOI: https://doi.org/10.1371/journal.pone.0299992

Interpretive Summary: Arachis duranensis(A. duranensis) is a wild peanut species and the donor of the A genome of common cultivated peanut. This crop wild relative has been identified as a potential source of genes for resistance to biotic and abiotic stress. The present study conducted a comprehensive genetic analysis of virtually all accessions of A. duranensis maintained at the U.S. Department of Agriculture, Agricultural Research Service, National Plant Germplasm System, which span the entire geographic range of the species in its center of origin. Results revealed single nucleotide polymorphism markers that were associated with specific environments and with variable levels of resistance to leaf spot diseases. This information will allow peanut breeding programs to select prospective A. duranensis originated from specific environments where there is a high probability of finding genes of resistance to be incorporated into cultivated peanut.

Technical Abstract: The genetic diversity that exists in natural populations of Arachis duranensis, the wild diploid donor of the A subgenome of cultivated tetraploid peanut, has the potential to improve crop adaptability, resilience to major pests and diseases, and drought tolerance. Despite its potential value for peanut improvement, limited research has been focused on the association between allelic variation, environmental factors, and response to early (ELS) and late leaf spot (LLS) diseases. The present study implemented a landscape genomics approach to gain a better understanding of the genetic variability of A. duranensis represented in the ex-situ peanut germplasm collection maintained at the U.S. Department of Agriculture, which spans the entire geographic range of the species in its center of origin in South America. A set of 2810 single nucleotide polymorphism (SNP) markers allowed a high-resolution genome-wide characterization of natural populations. The analysis of population structure showed a complex pattern of genetic diversity with five putative groups. The incorporation of bioclimatic variables for genotype-environment associations, using the latent factor mixed model (LFMM2) method, provided insights into the genomic signatures of environmental adaptation, and led to the identification of SNP loci whose allele frequencies were correlated with elevation, temperature, and precipitation-related variables (q < 0.05). The LFMM2 analysis for ELS and LLS detected candidate SNPs and genomic regions on chromosomes A02, A03, A04, A06, and A08. These findings highlight the importance of the application of landscape genomics in ex situ collections of peanut and other crop wild relatives to effectively identify favorable alleles and germplasm for incorporation into breeding programs. We report new sources of A. duranensis germplasm harboring adaptive allelic variation, which have the potential to be utilized in introgression breeding for a single or multiple environmental factors, as well as for resistance to leaf spot diseases.