Breakdown of Self-Incompatibility in a Natural Population ofPetunia axillaris Caused by Loss of Pollen Function

Abstract

Although Petunia axillaris subsp. axillaris is described as a self-incompatible taxon, some of the natural populations we have identified in Uruguay are composed of both self-incompatible and self-compatible plants. Here, we studied the selfincompatibility (SI) behavior of 50 plants derived from such a mixed population, designated U83, and examined the cause of the breakdown of SI. Thirteen plants were found to be self-incompatible, and the other 37 were found to be selfcompatible. A total of 14 S-haplotypes were represented in these 50 plants, including two that we had previously identified from another mixed population, designated U1. All the 37 self-compatible plants carried either an S C1 -or an S C2 -haplotype. S C1 S C1 and S C2 S C2 homozygotes were generated by self-pollination of two of the self-compatible plants, and they were reciprocally crossed with 40 self-incompatible S-homozygotes (S 1 S 1 through S 40 S 40 ) generated from plants identified from three mixed populations, including U83. The S C1 S C1 homozygote was reciprocally compatible with all the genotypes examined. The S C2 S C2 homozygote accepted pollen from all but the S 17 S 17 homozygote (identified from the U1 population), but the S 17 S 17 homozygote accepted pollen from the S C2 S C2 homozygote. cDNAs encoding S C2 -and S 17 -RNases were cloned and sequenced, and their nucleotide sequences were completely identical. Analysis of bud-selfed progeny of heterozygotes carrying S C1 or S C2 showed that the SI behavior of S C1 and S C2 was identical to that of S C1 and S C2 homozygotes, respectively. All these results taken together suggested that the S C2 -haplotype was a mutant form of the S 17 -haplotype, with the defect lying in the pollen function. The possible nature of the mutation is discussed.Naturally occurring or induced (e.g. by radiation) self-compatible mutants of self-incompatible species in the Solanaceae have provided useful materials for studying the mechanism of the S-RNase-mediated self-incompatibility (SI) system. For example, molecular genetic studies of a self-compatible line of Lycopersicon peruvianum have suggested that the RNase activity of S-RNases is an integral part of the SI mechanism because mutations in the S-RNase gene rendering its protein product without the RNase activity cause the breakdown of SI (Kowyama et al., 1994a;Royo et al., 1994). Moreover, cytological and molecular genetic studies of x-ray irradiationinduced self-compatible mutants have uncovered a phenomenon, called competitive interaction, where duplication of the S-locus region renders pollen grains carrying two different pollen S-alleles unable to function in SI (de Nettancourt, 1977;Golz et al., 2000). Studies of self-compatible mutants have also led to the identification of loci unlinked to the S-locus that are required for the function of the S-RNase gene or the yet unidentified pollen S-gene. For example, mutations in the HT gene, which encodes a small Asn-rich protein (McClure et al., 1999), are partially responsible for the breakdown o...

Segregation Analyses of Partial Self-Incompatibility in Self and Cross Progeny of Solanum carolinense Reveal a Leaky S-Allele

“…In Campanula rapunculoides, analyses of 31 parental families suggested the presence of 3-5 unlinked, mostly recessive genetic modifiers affecting the strength of the SI response (GoodAvila and Stephenson 2002). In P. axillaris, the presence of self-compatible plants has been shown to be due to three different mechanisms: a linked gene that suppresses the expression of a specific S-RNase gene (Tsukamoto et al 2003a), a loss of function on the pollen component of SI (Tsukamoto et al 2003b), and the presence of unlinked modifiers (Tsukamoto et al 1999). The variable strength of SI has been shown in most cases in species with small patchy populations such as weeds (Baker 1965), island colonizers (Bateman 1952;Burd 1994), and populations growing in peripheral habitats (Busch 2005); these populations typically undergo repeated events of colonization and local extinction and usually consist of a small number of individuals and are likely to experience reduced pollinator and mate availability.…”

“…One possible target may lie on the flanking regions surrounding different S-alleles. These sequences are known to be highly divergent (Coleman and Kao 1992); therefore, it could be possible for specific regulatory proteins to be either required for the appropriate transcription of different S-alleles or involved in the turnover of specific RNA transcripts (Tsukamoto et al 2003a).…”

The Molecular and Genetic Bases of S-RNase-Based Self-Incompatibility

“…One possible role of the modifier genes is to regulate the expression of the S-locus genes. For example, Tsukamoto et al (1999Tsukamoto et al ( , 2003 found that several pistil-part self-compatible plants identified from a natural population of self-incompatible Petunia axillaris carried a defective S 13 -haplotype (designated S 13 sps ), which did not produce any transcript of the S 13 -RNase gene. They further showed that self-incompatible progeny homozygous or heterozygous for the functional S 13 -haplotype were obtained from self-pollination of the self-compatible plants that carried the S 13 sps S 15 genotype.…”

Phylogenetic Relationship between Degree of Self-compatibility and Floral Traits in Lilium longiflorum Thunb. (Liliaceae)

“…The system can be lost secondarily, resulting in transition to self-compatibility (SC) by mutations linked to the Slocus (Broothaerts et al, 2004;de Nettancourt, 2001), by the presence of pollen heteroallelic for the Sgenotype, which may be the result of polyploidization (Entani et al, 1999), or by modifier gene(s) unlinked to the S-locus (Tsukamoto et al, 2003).…”