Gametophytic Self-Incompatibility: A Mechanism for Self/Nonself Discrimination during Sexual Reproduction

Various mechanisms in flowering plants have evolved to prevent the tendency of self-fertilization created by close proximity of male and female reproductive organs in a perfect flower. One such mechanism, called self-incompatibility (SI), allows the pistil of a plant to reject self pollen or pollen from genetically related individuals, thus preventing inbreeding and promoting outcrosses. Genetic studies carried out early in this century led to the identification of two different types of SI: gametophytic self-incompatibility (GSI) and sporophytic self-incompatibility (SSI). GSI was first studied in the Solanaceae family, and SSI was first studied in the Cruciferae family. To date, these two families still remain the best characterized for their respective SI systems. In both families, SI is controlled by a multiallelic locus termed the S-locus. For GSI, the SI behavior of the pollen is determined by the genotype of the pollen grain itself, whereas for SSI, the SI behavior of the pollen is determined by the genotype of the pollen parent. This difference most likely reflects the difference in the site of expression of the pollen S-allele: microspores for GSI and tapetal tissue for SSI (de Nettancourt, 1977). In the case of SSI, depending on the S-allele combination, the two S-allele specificities displayed by the pollen may be co-dominant or may exhibit other relationships such as dominance or mutual weakening (de Nettancourt, 1977). Figure 1 illustrates the difference in the SI behavior of SSI and GSI, assuming co-dominance of S-alleles in the pollen for SSI. Crosses between an SlS2 plant (female) and an SIS3 plant (male) will be compatible if the species displays GSI and will be incompatible if the species displays SSI. The reasons are as follows. In the case of GSI, the SI phenotypes of Si and S3 pollen produced by the SIS3 plant are Si and S3, respectively. The pollen bearing S-allele is rejected by the pistil of the SlS2 plant because of the matching of the Siallele, whereas the pollen bearing S3-allele, an allele different from those carried by the pistil, is able to effect fertilization to produce SlS3 or S2S3 progeny. The rejection of incompatible pollen usually occurs after the pollen has germinated and grown into the style. In the case of SSI, both Si and S3 pollen behave genetically as if they bear both Siand S3-alleles. Since the S1-allele is also carried by the pistil, neither pollen is able to effect fertilization. The rejection of incompatible pollen usually occurs on the surface of the stigma. Interest in SI largely lies, on the one hand, in its use as a model system to study cell-cell communication, and, on the other hand, in exploring its potential applications in hybrid seed production. Studies prior to 1980 focused mostly on the physiological, cytological, and genetic aspects. A detailed account of the large volume of early work can be found in a monograph by de Nettancourt (1977). Molecular biological studies of SI began in the early 1980s and have resulted in substantial progress toward understanding the molecular and biochemical bases of both GSI and SSI. Through the work of the last decade, it has become clear that GSI and SSI differ not only in the genetic determinant of pollen behavior, but also in the mechanism of SI interactions. This paper will not address the SSI system, but will focus mostly on recent molecular biological studies of GSI in the Solanaceae family.