Adaptive and maladaptive introgression in grapevine domestication

Authors: XIAO, HUA - Chinese Academy Of Agricultural Sciences; LIU, ZONGJIE - Chinese Academy Of Agricultural Sciences; WANG, NAN - Chinese Academy Of Agricultural Sciences; LONG, Q - Chinese Academy Of Agricultural Sciences; CAO, SHUO - Chinese Academy Of Agricultural Sciences; HUANG, GUIZHOU - Chinese Academy Of Agricultural Sciences; LIU, WENWEN - Chinese Academy Of Agricultural Sciences; PENG, YANLING - Chinese Academy Of Agricultural Sciences; Riaz, Summaira; WALKER, M - University Of California, Davis; GAUT, BRANDON - University Of California Irvine; ZHOU, YONGFENG - Chinese Academy Of Agricultural Sciences

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2023
Publication Date: 6/5/2023
Citation: Xiao, H., Liu, Z., Wang, N., Long, Q., Cao, S., Huang, G., Liu, W., Peng, Y., Riaz, S., Walker, M.A., Gaut, B.S., Zhou, Y. 2023. Adaptive and maladaptive introgression in grapevine domestication. Proceedings of the National Academy of Sciences (PNAS). 120(24). Article e2222041120. https://doi.org/10.1073/pnas.2222041120.
DOI: https://doi.org/10.1073/pnas.2222041120

Interpretive Summary: Mideast was the first center of domestication of cultivated grapes (Vitis vinifera ) from its wild progenitor Vitis sylvestris. Previous studies identified genomic signals of introgression in cultivated grapes. This study tackles the biological effects of introgression that impact disease resistance, aromatic compounds and other quality measures. Study identified continued gene flow between European wild grapes and cultivated grapes with dominant soft selective sweeps for artificial selection of genes in the pathway of aromatic compounds and disease resistance. Higher deleterious burden was identified in introgression fragments. Over all, identification of genomic regions that contribute to genetic load will help grape breeders to make informed decisions by selecting lines with minimum deleterious alleles.

Technical Abstract: After being domesticated in Mideast, grapes spread to Europe around three thousand years ago. Previous studies observed genomic signals of introgression from wild grapes to cultivated ones, however, the mode and biological effects of such introgression events were still unknown. Understanding these processes is critical for genomic breeding to take advantage of the wild resources. Based on population genomic analysis, we found gene flow continually between European wild grapes (EU) and cultivated grapes in the past ~1000 years, especially from EU to wine population using deep resequencing data of 345 samples spanning the distributional range of the wild (Vitis vinifera ssp. sylvestris) and cultivated (Vitis vinifera ssp. vinifera) grapes. Machine learning-based population genetic analyses indicated that soft selective sweeps were dominant in the signals of artificial selection and the gene pathways associated with the synthesis of aromatic compounds and disease resistance were enriched in introgression regions underlying positive selection. The EU wild grapes were used as important resources for improving the flavor and resistance in cultivated grapes. Despite the potential benefits of introgression in crop improvement, it should be noted, a higher deleterious burden was identified in introgression fragments, and most of the deleterious single nucleotide polymorphisms (SNPs) and structure variants (SVs) were hidden in a heterozygous state aggregating the genetic load due to clonal propagation. In general, the cultivated grapes got benefit from the introgression of wild grapes, but it also increases the genetic load for future grapevine breeding.