The spinach YY genome reveals sex chromosome evolution, domestication, and introgression history of the species

Authors: MA, XIAOKAI - Fuijan Agricultural University; YU, LI'ANG - Fuijan Agricultural University; FATIMA, MAHPARA - Fuijan Agricultural University; WADLINGTON, WILLIAM - University Of Illinois; Hulse-Kemp, Amanda; ZHANG, XINGTAN - Fuijan Agricultural University; ZHANG, SHENGCHENG - Fuijan Agricultural University; XU, XINDAN - Fuijan Agricultural University; WANG, JINGJING - Agriculture And Forestry University(AFU); HUANG, HUAXING - Agriculture And Forestry University(AFU); LIN, JING - Agriculture And Forestry University(AFU); DENG, BAN - Agriculture And Forestry University(AFU); LIAO, ZHENYANG - Agriculture And Forestry University(AFU); YANG, ZHENHUI - Agriculture And Forestry University(AFU); MA, YANHONG - Agriculture And Forestry University(AFU); TANG, HAIBAO - Agriculture And Forestry University(AFU); VAN DEYNZE, ALLEN - University Of California; MING, RAY - University Of Illinois

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/16/2022
Publication Date: 3/7/2022
Citation: Ma, X., Yu, L., Fatima, M., Wadlington, W.H., Hulse-Kemp, A.M., Zhang, X., Zhang, S., Xu, X., Van Deynze, A., Ming, R. 2022. Sex chromosome evolution, domestication and introgression history revealed by a YY genome in spinach. Genome Biology. https://doi.org/10.1186/s13059-022-02633-x.
DOI: https://doi.org/10.1186/s13059-022-02633-x

Interpretive Summary: Spinach is a plant that exhibits a unique system that has male and female plants, determined by a sex chromosome system with X and Y chromosomes. A female was previously sequenced, but a male has never been sequenced to investigate the differences between the sex chromosomes. In this study we sequenced a male spinach plant and were able to look at how the Y chromosome came to be in spinach. It appears that the Y chromosome evolved from a normal non-sex chromosome by an event that caused a large section of genes to become reoriented, or inverted in order. Using analytical techniques we were able to determine that this likely happened about 1.92 million years ago and was accompanied by many other changes, particularly in repetitive sequences. We also investigated the genetic information from 112 other spinach lines which allowed us to determine that spinach domestication likely occurred about 7,000 years earlier than the last estimate. These lines were also useful to help pinpoint genetic regions that may be important for disease resistance, leaf shape and flowering time.

Technical Abstract: Background: Spinach is dioecious with an XY sex chromosome system, but the Y chromosome has not been sequenced. As a global vegetable crop, its genomic history of domestication and improvement remain limited. Results: A high-quality YY genome was assembled into 948 Mb with 26,910 annotated genes. Genetic mapping defined a 38.18 Mb sex determination region (SDR) oin chromosome 1. The nascent sex chromosome in spinach evolved from an autosome by a large inversion containing sex determination genes about 1.92 Mya companying companied bywith a burst of an SDR-specific repeats burst (0.1-0.15 Mya). A recent genus-specific repeats burst (0-0.025 Mya), explained the large SDR and the highly repetitive genome (74%). One Y-specific gene, NRT1/PTR 6.4 involved in reproductive-organ initiation, initiation and is defined as a strong candidate for sex determination. Resequencing 112 genomes revealed a severe domestication bottleneck at ~10.87 Kya followed by 4300 years of pre-domestication, which dated spinach domestication 7000 years earlier than the archeological record. A strong selection signal associated with internode elongation and leaf area expansion could be related to domestication of edible traits domestication. Several strong intra- and inter-specific genomic introgressions from two wild species, S. turkestanica and S. tetrandra, related to downy mildew resistance (e.g. RAR), cold acclimation (e.g. frost-resistant STS1 etc.), leaf morphology, and flowering time shift likely contributed to spinach improvement. Conclusions: Our findings yield new knowledge for understanding spinach sex-determination mechanisms and provide genomic resources for spinach improvement.