The Diversity and Dynamics of Sex Determination in Dioecious Plants

Abstract

The diversity of inflorescences among flowering plants is captivating. Such charm is not only due to the variety of sizes, shapes, colors, and flowers displayed, but also to the range of reproductive systems. For instance, hermaphrodites occur abundantly throughout the plant kingdom with both stamens and carpels within the same flower. Nevertheless, 10% of flowering plants have separate unisexual flowers, either in different locations of the same individual (monoecy) or on different individuals (dioecy). Despite their rarity, dioecious plants provide an excellent opportunity to investigate the mechanisms involved in sex expression and the evolution of sex-determining regions (SDRs) and sex chromosomes. The SDRs and the evolution of dioecy have been studied in many species ranging from Ginkgo to important fruit crops. Some of these studies, for example in asparagus or kiwifruit, identified two sex-determining genes within the non-recombining SDR and may thus be consistent with the classical model for the evolution of dioecy from hermaphroditism via gynodioecy, that predicts two successive mutations, the first one affecting male and the second one female function, becoming linked in a region of suppressed recombination. On the other hand, aided by genome sequencing and gene editing, single factor sex determination has emerged in other species, such as persimmon or poplar. Despite the diversity of sex-determining mechanisms, a tentative comparative analysis of the known sex-determining genes and candidates in different species suggests that similar genes and pathways may be employed repeatedly for the evolution of dioecy. The cytokinin signaling pathway appears important for sex determination in several species regardless of the underlying genetic system. Additionally, tapetum-related genes often seem to act as male-promoting factors when sex is determined via two genes. We present a unified model that synthesizes the genetic networks of sex determination in monoecious and dioecious plants and will support the generation of hypothesis regarding candidate sex determinants in future studies.

Genome-Wide Association Studies for Sex Determination and Cross-Compatibility in Water Yam (Dioscorea alata L.)

“…The presence of gene/protein families regulating hormones such as gibberellins, auxins, ethylene and cytokinins in the sex-determining regions ( Supplementary Table S3 ) could confirm the crucial roles played by these phytohormones for sex determination in dioecious and monoecious plants. Generally, auxins and ethylene have feminizing effects, whereas cytokinins and gibberellins have masculinizing effects [ 15 , 21 , 31 , 32 , 33 ]. A better understanding of the hormone balance for a sex phenotype display could facilitate manipulation of flowering behaviors and sex ratios in D. alata .…”

“…The most popular gene/protein families with direct or indirect influence on sex determination or with differential expression among sexes or those regulating hormones linked to sex ratio bias in other plant species are listed below. These are: Zinc finger, RING/FYVE/PHD-type [ 46 ]; Glycosyltransferase AER61 [ 47 ]; NAD(P)H-quinone oxidoreductase subunit L [ 48 ]; GLABROUS1 enhancer-binding protein [ 49 ]; Auxin efflux carrier [ 50 ]; Ribosomal protein PSRP-3/Ycf65 [ 15 ]; MADS-box [ 51 , 52 , 53 ]; Myb/SANT-like domain [ 54 ]; Aldolase-type TIM barrel [ 55 ]; NAD(P)-binding domain [ 56 ]; Zinc finger, Rad18-type putative [ 57 ]; Tify [ 50 , 58 ]; ABC transporter-like [ 59 , 60 ]; Homeodomain-like [ 61 , 62 ]; Prohibitin [ 63 ]; Initiation factor eIF-4 gamma, MA3 [ 64 ]; and HD-ZIP protein, N-terminal [ 65 ].…”

“…The genetic mechanisms range from a single locus to sex chromosomes bearing several linked loci required for sex determination [ 12 , 13 ]. Dioecy in plants is inherited via three sex chromosome systems: XX/XY, XX/X0 and WZ/ZZ, such that XX or WZ determines female sex phenotype and XY, X0 or ZZ the male sex phenotype [ 12 , 13 , 14 , 15 ]. Most of the studied yam species, such as D. alata [ 3 , 5 ], D. floribunda [ 16 ], and D. tokoro [ 17 ] are characterized by the male heterogametic (XX/XY) sex-determination system.…”

Integrative genomics reveals paths to sex dimorphism in Salix purpurea L

“…The XY system, where the male is the heterogametic sex, tends to be more prevalent, and is found in 84.7% of diecious angiosperm species, including Asparagus officinalis , Carica papaya , Diospyros , and Phoenix dactylifera . In the less common ZW system, females are heterogametic, as in Fragaria and Silene otitis 10 , 11 . The Salicaceae family is of particular interest for use as a model in understanding the evolution of sex chromosomes and sex determination in plants, because the family is almost exclusively diecious, yet the sex determination region (SDR) has been remarkably dynamic 4 , 12 , 13 .…”

“…Differing sex determination systems (as a result of sex chromosome turnover) in closely related taxa have been observed across both plants and animals. For instance, both XY and ZW systems are represented in Silene 10 , 11 . In cichilid fish, multiple sex determination loci and systems have been identified in specific populations 20 .…”