Loss of a histidine residue at the active site of S-locus ribonuclease is associated with self-compatibility in Lycopersicon peruvianum.

Abstract

Gametophytic self-incompatibility in the Solanaceae is controlled by a single, nultiafleic locus, the S locus.We have recently described an allele of the S locus of Lycopersicon peruvianum that caused this normally self-incompatible plant to become self-compatible. We have now characterized two glycoproteins present in the styles of self-compatible and self-incompatible accessions of L. peruvianum: one is a ribonuclease that cosegregates with a functional self-incompatibility allele (S6 allele); the other cosegregates with the self-compatible allele (S, allele) but has no ribonuclease activity. The derived amino acid sequences of the cDNAs encoding the S6 and Sc glycoproteins resemble sequences of other ribonucleass encoded by the S locus. The derived sequence for the S. glycoprotein differs from the others by lacking one of the hidine residues found in all other S-locus ribonucleases. These findings demonstrate the essential role of ribonuclease activity in self-incompatibility and lend further weight to evidence that this hisidine residue is involved in the catalytic site of the enzyme.Self-incompatibility is a major factor affecting mating systems in flowering plants (1, 2). In plants with gametophytic self-incompatibility such as members of the Solanaceae, rejection or acceptance of pollen tubes by the style is controlled by a single, multiallelic locus, the S locus. Pollen expresses its haploid S genotype, and matings are incompatible if the S allele of the pollen is matched by one of the two alleles expressed in the pistil. Thus, self-incompatibility is an example of recognition between plant cells; the underlying mechanism may be similar to other recognition systems in plants such as those involved in host-pathogen interactions (3, 4). The products of the S locus are a class of extracellular glycoproteins with RNase activity called S-RNases (5, 6). The genes that encode these proteins cosegregate with alleles of the S locus (7, 8). S-RNases are abundant proteins found in high concentrations in the transmitting tract of the style, the site at which inhibition of pollen tubes occurs during incompatible matings (9). Sequences of S-RNase alleles from different solanaceous species share a characteristic structure that includes five short stretches of highly conserved sequence (10). Two of these conserved regions correspond to the sequences surrounding the catalytic domains of fungal RNases and include both of the histidine residues essential for catalytic activity (11 LA2157 is self-compatible and has S genotype SS,; LA2163 is self-incompatible and has the S genotype 56S7 (16). L. peruvianum plants homozygous for the S6 allele were produced by self-pollinating heterozygous individuals at the green bud stage as described (16).Purification and N-Terminal Sequencing of the S6 and S, Glycoproteins. Extracts from 50 styles of plants homozygous for the S6 or S, alleles were prepared and fractionated by cation-exchange chromatography as described (18). S glycoproteins recovered from the extract after ammonium...

Structural and Transcriptional Analysis of the Self-Incompatibility Locus of Almond: Identification of a Pollen-Expressed F-Box Gene with Haplotype-Specific Polymorphism

“…S-RNase is a basic glycoprotein with RNase activity (McClure et al, 1989). RNase activity of S-RNase is required for the pistil to reject self-pollen Royo et al, 1994;McCubbin et al, 1997). The rRNA of incompatible pollen of Nicotiana alata is degraded in the style, consistent with a model postulating that the S-RNases act as intracellular cytotoxins (McClure et al, 1990).…”

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

“…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).…”

Self-Incompatibility System of Ipomoea trifida, a Wild-Type Sweet Potato

“…The original S -allele is unknown; however, the fact that the Sc haplotype is within the dominant-recessive hierarchy suggests that Sc lacks one or more genes that contribute to SI but maintains genes that contribute to determination of dominance among S -haplotypes. Analyses of Sc mutants have provided important information for understanding the genetic features of SI in Brassica (Watanabe et al 1997 ), Pyrus (Sassa et al 1997 ), Solanum (Royo et al 1994 ), and other plant species. In the case of Ipomoea , analyzing the Sc mutant may provide information to allow elucidation of the genetic features of SI.…”