Speciation genes in plants

Abstract

Background: Analyses of speciation genes--genes that contribute to the cessation of gene flow between populations--can offer clues regarding the ecological settings, evolutionary forces and molecular mechanisms that drive the divergence of populations and species. This review discusses the identities and attributes of genes that contribute to reproductive isolation (RI) in plants, compares them with animal speciation genes and investigates what these genes can tell us about speciation.

Scope: Forty-one candidate speciation genes were identified in the plant literature. Of these, seven contributed to pre-pollination RI, one to post-pollination, prezygotic RI, eight to hybrid inviability, and 25 to hybrid sterility. Genes, gene families and genetic pathways that were frequently found to underlie the evolution of RI in different plant groups include the anthocyanin pathway and its regulators (pollinator isolation), S RNase-SI genes (unilateral incompatibility), disease resistance genes (hybrid necrosis), chimeric mitochondrial genes (cytoplasmic male sterility), and pentatricopeptide repeat family genes (cytoplasmic male sterility).

Conclusions: The most surprising conclusion from this review is that identities of genes underlying both prezygotic and postzygotic RI are often predictable in a broad sense from the phenotype of the reproductive barrier. Regulatory changes (both cis and trans) dominate the evolution of pre-pollination RI in plants, whereas a mix of regulatory mutations and changes in protein-coding genes underlie intrinsic postzygotic barriers. Also, loss-of-function mutations and copy number variation frequently contribute to RI. Although direct evidence of positive selection on speciation genes is surprisingly scarce in plants, analyses of gene family evolution, along with theoretical considerations, imply an important role for diversifying selection and genetic conflict in the evolution of RI. Unlike in animals, however, most candidate speciation genes in plants exhibit intraspecific polymorphism, consistent with an important role for stochastic forces and/or balancing selection in development of RI in plants.

Fig. 1.

Reproductive isolating barriers occur at multiple prezygotic and postzygotic life-history stages.

Fig. 2.

Diverse evolutionary paths lead to the origin of Dobzhansky–Muller incompatibilities in plants. (A) Two substitutions within a single lineage illustrated by Cf-2 and RCR3 loci in Solanum species. (B) Divergent resolution of an ancestral gene duplication as illustrated by the HPA1 and HPA2 loci in Arabidopsis thaliana populations. (C) Divergent resolution of an ancestral polymorphism at one locus and lineage-specific substitution at a second tightly linked locus as illustrated by the SaF and SaM loci in domesticated Oryza sativa subspecies.

Fig. 3.

Two evolutionary scenarios for the spread of CMS and RF alleles in hermaphroditic populations. (A) Mitochondrial CMS-causing allele arises first, followed by evolution of a new nuclear restorer allele. (B) Invasion of a CMS allele in a population segregating for RF and rf alleles. Females and hermaphrodites are represented by standard symbols. Frequencies of the female permissive alleles at the mitochondrial CMS locus and nuclear restorer locus are shown in pink.