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other·plant_genetics, crop_science, genomics, agriculture, evolutionary_biology·PMC10179502

Historical Selection, Adaptation Signatures, and Ambiguity of Introgressions in Wheat

International Journal of Molecular Sciences · 8 authors, 3 centres

AI SUMMARY

FIDELITY 100%

POPULATION921 wheat accessions (exome capture dataset) including landraces, cultivars, and breeding materials; plus a whole-genome resequencing dataset of various Triticum species and wild relatives.

INTERVENTIONGenome-wide scans (PC-based, FST, PhiPT) and genome-environment association (GEA) analyses to detect adaptive signatures and trace introgression origins.

COMPARISONGenetic differentiation and ancestry comparisons among subpopulations defined by geography (e.g., Australian, Mediterranean, Former Soviet Union, Old World) and among wheat types (e.g., hexaploid cultivars, landraces, durum, wild emmer, spelt, macha, Indian dwarf).

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TL;DR

This study analyzed genome-wide SNP data from over 900 wheat accessions to identify adaptive genetic signatures and the origin of a previously reported introgression on chromosome 4A. The authors found that a highly differentiated region on chromosome 4A dichotomizes wheat populations into two groups, with one group (G2) enriched in landraces from the Mediterranean and Old World regions. Contrary to prior claims of direct wild emmer introgression, the evidence suggests the 4A signature in modern cultivars likely originated from cultivated wheat types, possibly linked to the Norin-10 semidwarf lineage, with implications for understanding wheat adaptation and breeding history.

Full summary

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**Background:** Wheat (Triticum sp.) underwent severe genetic bottlenecks from polyploidization, domestication, and the transition to free-threshing grain, yet it adapted to a vast range of environments. Understanding the genetic basis of this adaptation and the origins of introgressed segments is important for breeding. A previous study (He et al.) identified a large introgression on chromosome 4A from wild emmer wheat, but the authors hypothesized it might instead derive from the Norin-10 semidwarf cultivar lineage.

**Methods:** Two SNP datasets were used: (1) exome capture data (~8.7M SNPs, filtered to ~113K SNPs, 921 accessions) from TriticeaeToolbox, and (2) whole-genome resequencing data (~100M SNPs) from Genome Variation Map. Population structure was assessed via ADMIXTURE, PCA, and neighbor-joining phylogeny. Genome scans for selection signatures used PCADAPT. Genome-environment association (GEA) was performed with LFMM2 using latitude, temperature, and earth skin temperature data for 113 landraces with coordinates. Candidate genes within 200 kb of significant loci were annotated via WheatGmap, Phytozome, and literature. To trace the 4A introgression origin, FST, PhiPT, and G-tests were computed for the most significant 5000 SNPs in the 4A region across diverse wheat types and wild relatives.

**Key Results:** Population structure revealed eight subpopulations (K=8) in the full dataset and seven in the landrace subset, largely reflecting geography. The largest genetic differentiation (FST = 0.34) was between Former Soviet Union (FSV) and Old World (OLDWP) subpopulations. Genome scans identified a highly differentiated region on chromosome 4A spanning ~174–465 Mb, plus outlier loci on chromosomes 2A, 5A, 6A, 7B, 1B, 4B, 5D, 7A, and 7D. Within the 4A region, 62 extreme outlier SNPs (p < 1 × 10⁻⁷⁵⁰) dichotomized the population into two groups: G1 (dominated by haplotype 1, 560 individuals) and G2 (dominated by haplotype 2, 115 individuals). G2 included ~130–140 of 347 landraces and 250–260 of 921 total accessions, with higher frequency in Mediterranean and Middle East regions. Haplotype analysis identified eight haplotypes; Hap1 and Hap2 together represented 675 of 921 accessions. GEA identified nine loci associated with latitude or temperature (FDR < 0.05), including Chr7A:118327401 (p = 1.63 × 10⁻⁸) and Chr2A:344449220 (p = 4.44 × 10⁻⁷) associated with latitude and temperature, respectively. The 4A region harbored >25 seed dormancy genes, >30 flowering-time genes, and >50 abiotic stress response genes. Candidate adaptive genes included SIGA, RBR1, CIPK, AGL30, SIZ2, and GCR1. Crucially, FST and PhiPT analyses showed hexaploid cultivars and durum wheat had zero differentiation from wild emmer at the 4A region (FST = PhiPT = 0), but the G-test (10,000 Markov chains, 5000 iterations) strongly differentiated cultivars from wild emmer while cultivars remained undifferentiated from other cultivated types (Indian dwarf, Tibetan semi-wild, Xinjiang wheat, etc.). Ancestral proportion analysis (K=5) showed >95% shared ancestry between cultivars and wild emmer, but also with these other cultivated wheats. The landrace-spelt group formed a distinct clade with long branches, concentrated in the Mediterranean region.

**Clinical Implications:** While not a clinical study, this research has significant implications for crop science and food security. Identifying adaptive genomic regions and their origins can guide wheat breeding for climate resilience, particularly for traits like drought, heat, and cold tolerance, flowering time, and seed dormancy. The finding that the 4A introgression likely came from cultivated wheat rather than wild emmer refines our understanding of wheat breeding history and highlights the value of landraces and heritage cultivars as genetic resources. This can inform conservation strategies and the development of better-adapted wheat varieties for diverse environments.

PICO

PPOPULATION

921 wheat accessions (exome capture dataset) including landraces, cultivars, and breeding materials; plus a whole-genome resequencing dataset of various Triticum species and wild relatives.

IINTERVENTION

Genome-wide scans (PC-based, FST, PhiPT) and genome-environment association (GEA) analyses to detect adaptive signatures and trace introgression origins.

OOUTCOME

Identification of highly differentiated genomic regions (especially chromosome 4A: ~174–465 Mb), candidate adaptive genes, and evidence that the 4A 'introgression' in modern cultivars is more likely from cultivated wheat (e.g., Norin-10 lineage) than from wild emmer.

STUDY TYPE

other

SPECIALTY

plant_genetics

SUMMARISED BY

AI pipeline

FIDELITY CHECK

100% · A

ORIGINAL PAPER

PMC10179502

Historical Selection, Adaptation Signatures, and Ambiguity of Introgressions in Wheat

International Journal of Molecular Sciences

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ABSTRACT

Abstract Wheat was one of the crops domesticated in the Fertile Crescent region approximately 10,000 years ago. Despite undergoing recent polyploidization, hull-to-free-thresh transition events, and domestication bottlenecks, wheat is now grown in over 130 countries and accounts for a quarter of the world’s cereal production. The main reason for its widespread success is its broad genetic diversity that allows it to thrive in different environments. To trace historical selection and hybridization signatures, genome scans were performed on two datasets: approximately 113K SNPs from 921 predominantly bread wheat accessions and approximately 110K SNPs from about 400 wheat accessions representing all ploidy levels. To identify environmental factors associated with the loci, a genome–environment association (GEA) was also performed. The genome scans on both datasets identified a highly differentiated region on chromosome 4A where accessions in the first dataset were dichotomized into a group (n = 691), comprising nearly all cultivars, wild emmer, and most landraces, and a second group (n = 230), dominated by landraces and spelt accessions. The grouping of cultivars is likely linked to their potential ancestor, bread wheat cv. Norin-10. The 4A region harbored important genes involved in adaptations to environmental conditions. The GEA detected loci associated with latitude and temperature. The genetic signatures detected in this study provide insight into the historical selection and hybridization events in the wheat genome that shaped its current genetic structure and facilitated its success in a wide spectrum of environmental conditions. The genome scans and GEA approaches applied in this study can help in screening the germplasm housed in gene banks for breeding, and for conservation purposes. Keywords: wheat, genome scans, adaptation, genetic signatures, introgression

CITATION EXPORT

Demissew Sertse, Frank M You, Valentyna Klymiuk et al.. Historical Selection, Adaptation Signatures, and Ambiguity of Introgressions in Wheat. International Journal of Molecular Sciences. (2023). https://doi.org/10.3390/ijms24098390

AUTHORS

8 · 3 CENTRES

Demissew Sertse, Frank M You, Valentyna Klymiuk, Jemanesh K Haile, Amidou N’Diaye, Curtis J Pozniak, Sylvie Cloutier, Sateesh Kagale

1Aquatic and Crop Resource Development, National Research Council Canada, Saskatoon, SK S7N 0W9, Canada
2Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada; [email protected] (F.M.Y.); [email protected] (S.C.)
3Crop Development Centre, University of Saskatchewan, Saskatoon, SK S7N 5A8, Canada; [email protected] (V.K.); [email protected] (J.K.H.); [email protected] (A.N.); [email protected] (C.J.P.)