Self-incompatibility systems: barriers to self-fertilization in flowering plants

Abstract

Flowering plants (angiosperms) are the most prevalent and evolutionarily advanced group of plants. Success of these plants is owed to several unique evolutionary adaptations that aid in reproduction: the flower, the closed carpel, double fertilization, and the ultimate products of fertilization, seeds enclosed in the fruit. Angiosperms exhibit a vast array of reproductive strategies, including both asexual and sexual, the latter of which includes both self-fertilization and cross-fertilization. Asexual reproduction and self-fertilization are important reproductive strategies in a variety of situations, such as when mates are scarce or when the environment remains relatively stable. However, reproductive strategies promoting cross-fertilization are critical to angiosperm success, since they contribute to the creation of genetically diverse populations, which increase the probability that at least one individual in a population will survive given changing environmental conditions. The evolution of several physical and genetic barriers to self-fertilization or fertilization among closely related individuals is thus widespread in angiosperms. A major genetic barrier to self-fertilization is self-incompatibility (SI), which allows female reproductive cells to discriminate between "self" and "non-self" pollen, and specifically reject self pollen. Evidence for the importance of SI in angiosperm evolution lies in the highly diverse set of mechanisms used by various angiosperm families for recognition of self pollen tube development and preventing self-fertilization.

A Dual Role for the S-Locus Receptor Kinase in Self-Incompatibility and Pistil Development Revealed by an Arabidopsis rdr6 Mutation

“…Among the best-known physiological outbreeding devices are genetic self-incompatibility (SI) systems that prevent self-fertilization (Takayama and Isogai, 2005;Rea and Nasrallah, 2008). Although SI ensures that pollen cannot fertilize ovules on the same plant, it is often accompanied by additional adaptations in floral architecture that increase the chance of cross-pollen receipt, such as increased separation in stigma and anther heights that causes stigmas to protrude above the anthers, a trait known as stigma exsertion.…”

“…Most A. thaliana accessions have flowers in which the close proximity of stigmas and anthers favors self-pollination, and the species also lacks the SI system typical of selfincompatible members of the Brassicaceae (reviewed in Takayama and Isogai, 2005;Rea and Nasrallah, 2008). In particular, all A. thaliana accessions analyzed to date lack functional alleles of the two highly polymorphic genes that together form the SI specificity-determining S-locus haplotype or S haplotype Tang et al, 2007;Shimizu et al, 2008): the S-locus receptor kinase (SRK) gene, which encodes a single-pass transmembrane kinase displayed on the surface of stigma epidermal cells, and the S-locus cysteine-rich protein (SCR) gene, which encodes a small pollen coat-localized protein that is the ligand for SRK.…”

Molecular Characterization and Evolution of Self-Incompatibility Genes inArabidopsis thaliana:The Case of theScHaplotype

“…Within each S-locus haplotype (hereafter S haplotype), are two genes that determine specificity in the SI response: one gene encodes the stigma-expressed S-locus receptor kinase (SRK) and the other encodes the pollen coat-localized ligand for SRK, the S-locus cysteine-rich (SCR) protein. The SRK and SCR proteins are highly polymorphic and co-evolving proteins (Sato et al 2002) and their haplotype-specific interaction is responsible for the specific recognition and inhibition by the stigma epidermis of self-related pollen (i.e., pollen derived from the same flower, other flowers on the same plant, or plants expressing the same S haplotype) (reviewed in Rea and Nasrallah 2008). Consequently, an understanding of the genetic events associated with the switch to self-fertility in the A. thaliana lineage was sought through analysis of SRK and SCR sequences harbored by various A. thaliana geographical accessions (Kusaba et al 2001;Shimizu et al 2004Shimizu et al , 2008Sherman-Broyles et al 2007;Tang et al 2007;Boggs et al 2009a,b;Tsuchimatsu et al 2010) and comparisons to orthologous sequences from A. thaliana's close self-incompatible relatives A. lyrata and A. halleri (Bechsgaard et al 2006).…”

The ejaculatory biology of leafcutter ants

“…Such recognition systems have been found before, for example in seminal fluid -sperm interaction between meiotic drive carrying males and wild-type males in the stalk-eyed fly Cyrtodiopsis whitei (Fry and Wilkinson, 2004), in pollen tube formation in plants (e.g. Higashiyama, 2010;Rea and Nasrallah, 2008), and in cooperation between sperm in deer mice, where sperm cells of the same male tend to cluster to a higher extent than mixtures of sperm cells from related and unrelated males (Fisher and Hoekstra, 2010). Self/nonself recognition also seems to play a role in aggregation formation in the budding yeast Saccharomyces cerevisiae (Smukalla et al, 2008) and the social amoeba Dictyostelium discoideum (Queller et al, 2003).…”