Why should we study plant sex chromosomes?

Abstract

Understanding plant sex chromosomes involves studying interactions between developmental and physiological genetics, genome evolution, and evolutionary ecology. We focus on areas of overlap between these. Ideas about how species with separate sexes (dioecious species, in plant terminology) can evolve are even more relevant to plants than to most animal taxa because dioecy has evolved many times from ancestral functionally hermaphroditic populations, often recently. One aim of studying plant sex chromosomes is to discover how separate males and females evolved from ancestors with no such genetic sex-determining polymorphism, and the diversity in the genetic control of maleness vs femaleness. Different systems share some interesting features, and their differences help to understand why completely sex-linked regions may evolve. In some dioecious plants, the sex-determining genome regions are physically small. In others, regions without crossing over have evolved sometimes extensive regions with properties very similar to those of the familiar animal sex chromosomes. The differences also affect the evolutionary changes possible when the environment (or pollination environment, for angiosperms) changes, as dioecy is an ecologically risky strategy for sessile organisms. Dioecious plants have repeatedly reverted to cosexuality, and hermaphroditic strains of fruit crops such as papaya and grapes are desired by plant breeders. Sex-linked regions are predicted to become enriched in genes with sex differences in expression, especially when higher expression benefits one sex function but harms the other. Such trade-offs may be important for understanding other plant developmental and physiological processes and have direct applications in plant breeding.

Figure 1.

Examples of 3 different kinds of Y-linked regions observed in angiosperms with male heterogamety to illustrate concepts described in the text. The top diagram shows an X chromosome, which is similar to the ancestral state before genetic sex determination evolved; its centromere is indicated at the left (circle), with an adjoining pericentromeric region that rarely recombines. The 3 diagrams below show different types of “Y chromosomes,” with thin horizontal lines indicating recombining regions (PARs) and thick ones nonrecombining regions. The top Y is identical with the X (homomorphism), except for presence of a single male-determining factor, which is always heterozygous in males. In the second, the male-determining locus is within a small completely nonrecombining region that may include several other genes (which, again will always be heterozygous with the X in males); this situation is also likely to be classified as homomorphic because the differentiated region is a small part of the chromosome. The bottom diagram shows a strongly heteromorphic situation, with the male-determining locus in a large completely nonrecombining region across most of the chromosome arm, including the centromere, and a larger size of the arm, compared with the homologous X arm.

Figure 2.

De novo evolution of separate sexes in an initially hermaphrodite or monoecious species, reversions, and turnovers. A) The pathway involving an initial M —> m male-sterility mutation in the hermaphroditic ancestor (in a stamen-promoting factor, or SPF), and a second mutation (or succession of mutations), denoted by SuF, GSF, or SOFF, suppresses female functions and creates males. Close linkage is predicted between the 2 mutations that define the Y-linked region, as observed. B) The pathway leading to the “persimmon system” in which femaleness is due to a mutation that causes active suppression of maleness (not to a loss of function mutation causing male sterility) and in which the second mutation is an unlinked duplication that creates males by suppressing the action of the allele that created females. C) Reversion to co-sexuality is possible under the Silene system by simple loss of the femaleness suppressor function, but in the persimmon system this is less likely (see main text), though turnover events can occur. In the pathway shown in part D, a new M factor can appear on any chromosome, including one that was an autosome in the ancestrally dioecious population, or in a new location on a sex chromosome. It can appear by transposition, inserting a duplicate of a progenitor gene from an ancestral location into a new one, or by in situ change of a gene, by a mutation that produces a male-determining function.

Figure 3.

Mechanisms causing lack of recombination. As in Figs. 1 and 2, thin horizontal lines indicate chromosome arms, and thick bars that include the male-determining factors indicate complete Y linkage. A) Recombination suppression events creating an old evolutionary stratum. The event may involve inversion of part of the chromosome (the X or the Y, as shown), or control by a genetic recombination modifier. B) Evolution of a sex-determining locus in a pericentromeric region that already recombined rarely in 1 or both sexes. The processes in B and C can include turnovers causing appearance of a male-determining locus in a new genomic location. C) Insertion of a maleness factor creating a small Y-linked region (in a chromosome that remains morphologically similar to the X). The small Y-specific region may locally hinder recombination with the X.