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

Abstract

Background Spinach (Spinacia oleracea L.) is a dioecious species with an XY sex chromosome system, but its Y chromosome has not been fully characterized. Our knowledge about the history of its domestication and improvement remains limited. Results A high-quality YY genome of spinach is assembled into 952 Mb in six pseudo-chromosomes. By a combination of genetic mapping, Genome-Wide Association Studies, and genomic analysis, we characterize a 17.42-Mb sex determination region (SDR) on chromosome 1. The sex chromosomes of spinach evolved when an insertion containing sex determination genes occurred, followed by a large genomic inversion about 1.98 Mya. A subsequent burst of SDR-specific repeats (0.1–0.15 Mya) explains the large size of this SDR. We identify a Y-specific gene, NRT1/PTR 6.4 which resides in this insertion, as a strong candidate for the sex determination or differentiation factor. Resequencing of 112 spinach genomes reveals a severe domestication bottleneck approximately 10.87 Kya, which dates the domestication of spinach 7000 years earlier than the archeological record. We demonstrate that a strong selection signal associated with internode elongation and leaf area expansion is associated with domestication of edibility traits in spinach. We find that several strong genomic introgressions from the wild species Spinacia turkestanica and Spinacia tetrandra harbor desirable alleles of genes related to downy mildew resistance, frost resistance, leaf morphology, and flowering-time shift, which likely contribute to spinach improvement. Conclusions Analysis of the YY genome uncovers evolutionary forces shaping nascent sex chromosome evolution in spinach. Our findings provide novel insights about the domestication and improvement of spinach.

Genomic profiling of dioecious Amaranthus species provides novel insights into species relatedness and sex genes

“…Only until recently have the genes and the mechanisms involved in sex determination been elucidated for a few plant species [ 39 – 45 ]. For the amaranths, previous work on dioecy confirmed males of A. tuberculatus and A. palmeri are heterogametic and, thus, have an XY sex chromosome system [ 23 , 46 ].…”

A convergent mechanism of sex determination in dioecious plants: Distinct sex-determining genes display converged regulation on floral B-class genes

“…Multiple-omics studies on dioecious plants accelerate the discovery of sex-determining genes, supporting both the "twogene model" and "one-gene model" (Charlesworth, 2016;Renner, 2016). Recent findings from poplar (Leite Montalvão et al, 2022) and persimmon (Yang et al, 2019), as well as studies in other dioecious species (Wang and Zhang, 2017;Zhang et al, 2020;Liu et al, 2022;Ma et al, 2022), led us to propose a convergent model of plant sex determination. According to this model, the sex-determining genes may vary across divergent species, but they eventually converged into floral MADS-box genes, B-class genes, in particular, to determine sexuality.…”

“…F. hispida had an SDR-located FhAG2 gene which was identified as the putative sex-determining gene (Zhang et al, 2020). Spinacia oleracea contained a Y-specific gene NRT1/PTR6.4 that was considered to be a strong candidate for sex determination (Ma et al, 2022). More recently the gymnosperm species C. panzhihuaensis was reported to have one SDR-located sex-determining candidate CYCAS_034085 (Liu et al, 2022).…”

“…Speculatively, this model could be further extended to dioecious species that follow the "one-gene model." Recent genomics studies on spinach (Ma et al, 2022), cycad (Liu et al, 2022), and Banyan tree (Zhang et al, 2020) all identified only one SDR-located gene that showed a male-specific expression pattern (Table 1). Therefore, all these species probably follow the convergent model we proposed here.…”

Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach

“…The quantitative RT-PCR was done with ABI 7500 (Applied Biosystems, Foster City, California, USA) by using two-steps kits (TaKaRa Biotech Co., Dalian, China). Spinach gene ( GAPDH ) was used as an internal control to monitor our transcriptomic data internally and evaluate our results ( Chen et al., 2012 ; Ma et al., 2022 ). First-strand cDNA was synthesized by PrimeScripte RT reagent kit with genomic DNA Eraser (TaKaRa) following reverse transcription step according to providers’ guidelines.…”