Sex determination and sex chromosome evolution in land plants

Abstract

Linnaeus's very first opus, written when he was 22 years old, dealt with the analogy that exists between plants and animals in how they ‘propagate their species’, and a revised version with a plate depicting the union of male and female Mercurialis annua plants became a foundational text on the sexuality of plants. The question how systems with separate males and females have evolved in sedentary organisms that appear ancestrally bisexual has fascinated biologists ever since. The phenomenon, termed dioecy, has important consequences for plant reproductive success and is of commercial interest since it affects seed quality and fruit production. This theme issue presents a series of articles that synthesize and challenge the current understanding of how plants achieve dioecy. The articles deal with a broad set of taxa, including Coccinia , Ginkgo , Mercurialis , Populus , Rumex and Silene , as well as overarching topics, such as the field's terminology, analogies with animal sex determination systems, evolutionary pathways to dioecy, dosage compensation, and the longevity of the two sexes. In this introduction, we focus on four topics, each addressed by several articles from different angles and with different conclusions. Our highlighting of unclear or controversial issues may help future studies to build on the current understanding and to ask new questions that will expand our knowledge of plant sexual systems. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.

Structural variation of a sex‐linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

“…Notably, GATA15 has been shown to have a role in floral organ initiation and meristem formation in Arabidopsis (Ranftl et al ., 2016) and floral organ development in Lagerstroemia speciosa L. (Hu et al ., 2019), further supporting its role in sex determination. The defect in 94003 offers support for a two‐gene model of sex determination in S. purpurea , which is different from the single‐gene, ARR17 ‐mediated sex determination system identified in Populus (Müller et al ., 2020; Renner & Müller, 2022). In the S. purpurea two‐gene system, we suggest that ARR17 serves as an active suppressor of male floral development.…”

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

“…The rapid development of high-throughput sequencing techniques has enabled a full flourish of plant genomics. Sexdetermining genes have been identified based on combined genomic and experimental approaches in certain dioecious plants with both Type I and II flowers (Carey et al, 2021;Renner and Müller, 2022). Taken together, these findings make it possible for us to elucidate the mechanism of sex determination in dioecious plants.…”

“…In contrast, sex determination of several other dioecious plants (Table 1) is known to follow the "one-gene model" that was firstly reported in persimmon (Diospyros, Ebenaceae) (Akagi et al, 2014;Charlesworth, 2016;Renner and Müller, 2022). In this model, one single gene located at SDR is critical to determine the sex via an epistatic gene interaction, rather than physical linkage with downstream genes.…”

The rate of W chromosome degeneration across multiple avian neo-sex chromosomes

“…Sex chromosomes have evolved from autosomes numerous times in animals and plants 1 – 4 . Male heterogametic systems (XY systems) are more widespread than female heterogametic systems (ZW systems), and in both these systems the sex chromosome pair often (but not always) evolve recombination suppression and genetic differentiation 1 , 2 .…”