Phylogenomic discovery of deleterious mutations facilitates hybrid potato breeding

Authors: WU, YAOYAO - Chinese Academy Of Agricultural Sciences; LI, DAWEI - Chinese Academy Of Agricultural Sciences; HU, YONG - Chinese Academy Of Agricultural Sciences; LI, HONGBO - Chinese Academy Of Agricultural Sciences; RAMSTEIN, GUILLAUME - Aarhus University; ZHOU, SHAOQUN - Chinese Academy Of Agricultural Sciences; ZHANG, XINYAN - Chinese Academy Of Agricultural Sciences; BAO, ZHIGUI - Chinese Academy Of Agricultural Sciences; ZHANG, YU - Chinese Academy Of Agricultural Sciences; SONG, BAOXING - Peking University; ZHOU, YAO - Chinese Academy Of Agricultural Sciences; ZHOU, YONGFENG - Chinese Academy Of Agricultural Sciences; GAGNON, EDELINE - Technical University Of Munich; SARKINEN, TIINA - Royal Botanical Gardens; KNAAP, SANDRA - Natural History Museum - London; ZHANG, CHUNZHI - Chinese Academy Of Agricultural Sciences; STADLER, THOMAS - Eth Zurich; Buckler, Edward - Ed; HUANG, SANWEN - Chinese Academy Of Agricultural Sciences

Submitted to: Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/5/2023
Publication Date: 5/25/2023
Citation: Wu, Y., Li, D., Hu, Y., Li, H., Ramstein, G.P., Zhou, S., Zhang, X., Bao, Z., Zhang, Y., Song, B., Zhou, Y., Zhou, Y., Gagnon, E., Sarkinen, T., Knaap, S., Zhang, C., Stadler, T., Buckler IV, E.S., Huang, S. 2023. Phylogenomic discovery of deleterious mutations facilitates hybrid potato breeding. Cell. 186(11):2313-2328. https://doi.org/10.1016/j.cell.2023.04.008.
DOI: https://doi.org/10.1016/j.cell.2023.04.008

Interpretive Summary: Researchers are working on a new method of breeding potatoes to make the crop more resilient and easier to grow. Over time, harmful mutations have built up in the potato's genetic makeup, making it difficult to create strong and productive potato varieties. By studying the genetic history of related plants, we identified these harmful mutations. Surprisingly, potatoes with a high number of these harmful mutations can actually be better for breeding new varieties, even though they may not grow as well initially. Including this genetic information in the breeding process significantly improves the accuracy of predicting potato yield. This study provides valuable insights into the widespread occurrence and characteristics of harmful mutations in the potato genome and how they impact breeding efforts.

Technical Abstract: Hybrid potato breeding will transform the crop from a clonally propagated tetraploid to a seed-reproducing diploid. Historical accumulation of deleterious mutations in potato genomes has hindered the development of elite inbred lines and hybrids. Utilizing a whole-genome phylogeny of 92 Solanaceae and its sister clade species, we employ an evolutionary strategy to identify deleterious mutations. The deep phylogeny reveals the genome-wide landscape of highly constrained sites, comprising ~2.4% of the genome. Based on a diploid potato diversity panel, we infer 367,499 deleterious variants, of which 50% occur at non-coding and 15% at synonymous sites. Counterintuitively, diploid lines with relatively high homozygous deleterious burden can be better starting material for inbred-line development, despite showing less vigorous growth. Inclusion of inferred deleterious mutations increases genomic-prediction accuracy for yield by 24.7%. Our study generates insights into the genome-wide incidence and properties of deleterious mutations and their far-reaching consequences for breeding.