Review

Genetic polymorphism of self-incompatibility in flowering plants

Lycopersicon peruvianum has a gametophytic self-incompatibility (GSI) mechanism controlled by a single genetic locus (S locus) with multiple alleles. S RNases, an allelic series of abundant stylar proteins, are products of the S locus in L. peruvianum and other Solanaceous plants. We introduced a genomic clone for the Sll RNase from L. peruvianum into a self-compatible species (Nicotiana tabacum) to examine if the expression pattern in the heterologous plant mimics that in L. peruvianum. The resultant transgenic N. tabacum plants expressed the introduced gene at a high level in their styles, similar to the Sll gene expression in L. peruvianum. The Sll RNase gene was expressed in the style at a similar stage of flower development in both the transgenic tobacco plants and L. peruvianum, suggesting that the regulatory mechanism for S RNase gene expression is operating in a self-compatible heterologous plant. However, the transgenic plants did not show any morphological changes or altered pollination behaviour as a result of this expression. Unexpectedly, the Sll RNase transcript was also found in developing anthers and mature pollen of the transgenic plants although the expression level is much lower compared to that in stylar tissues. This expression pattern has not been observed in L. peruvianum.

Plants and fungi show an astonishing diversity of mechanisms to promote outbreeding, the most widespread of which is sexual incompatibility. Sexual incompatibility involves molecular recognition between mating partners. In fungi and algae, highly polymorphic mating-type loci mediate mating through complementary interactions between molecules encoded or regulated by different mating-type haplotypes, whereas in flowering plants polymorphic self-incompatibility loci regulate mate recognition through oppositional interactions between molecules encoded by the same self-incompatibility haplotypes. This subtle mechanistic difference is a consequence of the different life cycles of fungi, algae, and flowering plants. Recent molecular and biochemical studies have provided fascinating insights into the mechanisms of mate recognition and are beginning to shed light on evolution and population genetics of these extraordinarily polymorphic genetic systems of incompatibility.

The potential to exploit self-incompatibility (SI) in plant breeding and its attraction as a system in which to investigate the molecular basis of cell-cell recognition and signaling has resulted in it becoming one of the most intensively studied and exciting topics in plant biology. Much research has encompassed the molecular cloning of genes involved in SI; consequently many reviews of this subject have focused on this area. In this article we have attempted to strike a somewhat different balance, with the objective of giving as broad a picture of the topic of SI as is possible within the confines of a single article. We provide a comprehensive summary of the genetics and population genetics of SI and, in describing progress toward the elucidation of the molecular basis of SI, have surveyed a much wider range of species than has previously been reviewed.

Patterns of the self-incompatibility system have been more often described for hermaphroditic, entomophilous and short-lived plant species. Quercus ilex is a long-lived, monoecious, anemophilous and highly self-incompatible species. We used pollination experiments to investigate phenotypic responses of the self-incompatibility system. Flowers from 14 individuals of the same stand were hand-pollinated with self-pollen, cross-pollen from a single donor and a mixture of the two types. We observed a slower pollen tube growth and no or nearly no seed production after self-pollination. The more self-pollen tubes reach the style, the more flowers will stop their ovule development, resulting in a high flower abortion rate. In open pollination, pollen load is not a limiting factor, but incompatible pollen may reach stigma simultaneously or before compatible cross-pollen, which will induce an early abortion of flowers. When pollination is qualitatively and quantitatively effective, the regulation of seed production related to the resources availability acts by the late abortion of fruit.

Les systèmes d'auto-incompatibilité ont été plus fréquemment étudiés chez des espèces hermaphrodites, entomophiles et à courte génération. Quercus ilex est une espèce monoïque anémophile et à longue génération. Des pollinisations contrôlées ont été réalisées pour l'analyse des réponses phénotypiques du système d'auto-incompatibilité. Des fleurs de 14 individus ont été pollinisées avec de l'autopollen, de l'allopollen simple donneur et un mélange d'auto-et d'allopollen. Nous avons observé une plus lente croissance des tubes polliniques et peu ou pas de production de fruits après autopollinisation. Plus le nombre de tubes d'autopollen atteignant le style est élevé, plus la proportion d'avortements précoces des fleurs sera importante. En pollinisation libre, le pollen n'est pas un facteur limitant, néanmoins si du pollen incompatible atteint le stigmate avant ou en même temps que de l'allopollen compatible, il peut diminuer significativement la production de fruits par un avortement précoce des fleurs. Quand la pollinisation est assurée par du pollen compatible, la régulation de la production de fruits, compte tenu de la disponibilité des ressources, s'opère par un avortement tardif des fruits.