Domestication and selection footprints in Persian walnuts (Juglans regia)

Abstract

Walnut (Juglans) species are economically important hardwood trees cultivated worldwide for both edible nuts and high-quality wood. Broad-scale assessments of species diversity, evolutionary history, and domestication are needed to improve walnut breeding. In this study, we sequenced 309 walnut accessions from around the world, including 55 Juglans relatives, 98 wild Persian walnuts (J. regia), 70 J. regia landraces, and 86 J. regia cultivars. The phylogenetic tree indicated that J. regia samples (section Dioscaryon) were monophyletic within Juglans. The core areas of genetic diversity of J. regia germplasm were southwestern China and southern Asia near the Qinghai-Tibet Plateau and the Himalayas, and the uplift of the Himalayas was speculated to be the main factor leading to the current population dynamics of Persian walnut. The pattern of genomic variation in terms of nucleotide diversity, linkage disequilibrium, single nucleotide polymorphisms, and insertions/deletions revealed the domestication and selection footprints in Persian walnut. Selective sweep analysis, GWAS, and expression analysis further identified two transcription factors, JrbHLH and JrMYB6, that influence the thickness of the nut diaphragm as loci under selection during domestication. Our results elucidate the domestication and selection footprints in Persian walnuts and provide a valuable resource for the genomics-assisted breeding of this important crop. Author summary Walnut (Juglans) species are economically important hardwood trees. The Persian walnut as a woody nut crop is limited by an incomplete understanding of the diversity and spatial genetic structure of the species’ wild germplasm, and the relationship of the secondary germplasm pool of walnut (wild and landrace walnuts) to improved cultivars. To better understand walnut’s breeding, we sequenced the genomes of 309 walnut accessions from around the world. The results revealed core areas of genetic diversity of Persian walnut germplasm were southwestern China and southern Asia near the Qinghai-Tibet Plateau and the Himalayas. The genome-wide scan for selective sweeps, genome-wide association studies (GWAS), and expression analysis identified JrbHLH and JrMYB6 transcript factors related to the thickness of the diaphragm that were under selection during domestication. Our results elucidate the genetic diversity of walnut and its evolution as a species and a crop. We identified centers of wild genetic diversity that could contribute to breeding and sustainable improvement.