Heteromorphic Self-incompatibility System Research Articles

A hemizygous supergene controls homomorphic and heteromorphic self-incompatibility systems in Oleaceae

Self-incompatibility (SI) has evolved independently multiple times and prevents self-fertilization in hermaphrodite angiosperms. Several groups of Oleaceae such as jasmines exhibit distylous flowers, with two compatibility groups each associated with a specific floral morph.1 Other Oleaceae species in the olive tribe have two compatibility groups without associated morphological variation.2,3,4,5 The genetic basis of both homomorphic and dimorphic SI systems in Oleaceae is unknown. By comparing genomic sequences of three olive subspecies (Olea europaea) belonging to the two compatibility groups, we first locate the genetic determinants of SI within a 700-kb hemizygous region present only in one compatibility group. We then demonstrate that the homologous hemizygous region also controls distyly in jasmine. Phylogenetic analyses support a common origin of both systems, following a segmental genomic duplication in a common ancestor. Examination of the gene content of the hemizygous region in different jasmine and olive species suggests that the mechanisms determining compatibility groups and floral phenotypes (whether homomorphic or dimorphic) in Oleaceae rely on the presence/absence of two genes involved in gibberellin and brassinosteroid regulation.

Farmers’ unconscious incorporation of sexually-produced genotypes into the germplasm of a vegetatively-propagated crop (Oxalis tuberosa Mol.)

Clonal propagation and sexual reproduction have diametrically opposite effects on the genetic diversity of crops, permitting, respectively, the conservation of existing genotypes or the creation of new diversity. Oxalis tuberosa Mol. (‘‘oca’’) exhibits a heteromorphic selfincompatibility system and is traditionally propagated clonally but is capable of sexual reproduction. In this study we investigated the influence of sexual reproduction on the in situ genetic diversity of a vegetatively propagated crop, taking oca as a model plant. The occurrence of sexual reproduction in natural conditions and its use by farmers were studied through surveys and interviews, while the effect of sexual reproduction on the in situ genetic diversity was evaluated using microsatellite analysis. Plantlets issuing from sexual reproduction were encountered in five of the nine visited communities. The interviews indicated that six out of the nine interviewed farmers were likely, albeit unconsciously, incorporating clonal lineages issuing from sexual reproduction into their varieties. The microsatellite analysis indicated a strong effect of such incorporations on the genetic diversity of the plant varieties. Assignment tests confirmed the allogamy of oca. ‘‘Complex varieties’’, made up of individuals exhibiting genetically differentiated genotypes,weremost likely the result of recent crossing. Unconscious incorporation of newgenotypes into the cultivated oca germplasm is therefore highly likely, raising the question of its potential occurrence in other vegetatively propagated crops. These findings could have an important effect on the adaptive potential of oca, especially in light of the genetic erosion that threatens the crop

The evolution of plant reproductive systems: how often are transitions irreversible?

Flowering plants are characterized by striking variation in reproductive systems, and the evolutionary lability of their sexual traits is often considered a major driver of lineage diversification. But, evolutionary transitions in reproductive form and function are never entirely unconstrained and many changes exhibit strong directionality. Here, I consider why this occurs by examining transitions in pollination, mating and sexual systems, some of which have been considered irreversible. Among pollination systems, shifts from bee to hummingbird pollination are rarely reversible, whereas transitions from animal to wind pollination are occasionally reversed. Specialized pollination systems can become destabilized through a loss of pollinator service resulting in a return to generalized pollination, or more commonly a reliance on self-pollination. Homomorphic and heteromorphic self-incompatibility systems have multiple origins but breakdown to self-compatibility occurs much more frequently with little evidence for subsequent gains, at least over short time-spans. Similarly, numerous examples of the shift from outcrossing to predominant self-fertilization are known, but cases of reversal are very limited supporting the view that autogamy usually represents an evolutionary dead-end. The evolution of dioecy from hermaphroditism has also been considered irreversible, although recent evidence indicates that the occurrence of sex inconstancy and hybridization can lead to the origin of derived sexual systems from dioecy. The directionality of many transitions clearly refutes the notion of unconstrained reproductive flexibility, but novel adaptive solutions generally do not retrace earlier patterns of trait evolution.

Differences in fine-scale spatial genetic structure across the distribution range of the distylous forest herb Pulmonaria officinalis (Boraginaceae)

BackgroundGeographical ranges of plants and their pollinators do not always entirely overlap and it has been suggested that the absence of specialized pollinators at range margins may induce changes in mating systems. Because a species’ mating system is known to have a considerable effect on within-population pollen movement, the extent of fine-scale spatial genetic structure (SGS) can be expected to differ between populations located at different parts of their geographical range. To test this prediction, we compared the fine-scale SGS between two core and two disjunct populations of the distylous forest herb Pulmonaria officinalis. Because in disjunct populations of this species the heteromorphic self-incompatibility system showed relaxation in the long-styled morph, but not in the short-styled morph, we also hypothesized that the extent of fine-scale SGS and clustering differed between morphs.ResultsSpatial autocorrelation analyses showed a significant decrease in genetic relatedness with spatial distance for both core and disjunct populations with the weakest SGS found in one of the core populations (Sp = 0.0014). No evidence of stronger SGS in the long-styled morph was found in the center of the range whereas one disjunct population showed a significantly (P = 0.029) higher SGS in the long-styled morph (SpL = 0.0070) than in the short-styled morph (SpS = 0.0044).ConclusionsConsistent with previous analyses on distylous plant species, we found weak, but significant spatial genetic structure. However, the extent of SGS varied substantially between populations within regions, suggesting that population characteristics other than mating system (e.g. local pollinator assemblages, population history) may be as important in determining variation in SGS.

Structure of styles and pollen tubes of distylous Turnera joelii and T. scabra (Turneraceae): are there different mechanisms of incompatibility between the morphs?

We investigate the anatomy and fine structure of styles and pollen tubes of two distylous Turnera species, which possess a heteromorphic self-incompatibility system. We use fluorescence and transmission electron microscopy to provide the first description of the cellular aspects of pollen-pistil interactions and ultrastructural changes to pollen tubes during the self-incompatibility response of the morphs. No obvious ultrastructural differences occur between pistils and compatible pollen tubes. Conspicuous differences were, however, observed between incompatible pollen tubes of the morphs. Incompatible pollen tubes of the long-styled morph always appear to be intact, and pollen tube tips are often highly fluorescent when stained with aniline blue, a stain for callose. Swelling and loss of cristae of mitochondria, and circular rough endoplasmic reticulum, were observed for incompatible pollen tubes of the long-styled morph. For incompatible pollen tubes of the short-styled morph, the tube cell wall apex and plasma membrane often appear to be ruptured and no easily recognizable organelles, such as mitochondria, can be discerned. Our results clearly show ultrastructural differences between the morphs and support the hypothesis that different self-incompatibility mechanisms might operate between them.

Identification of genes showing differential expression between morphs in developing flowers of Primula vulgaris

Heteromorphic self-incompatibility systems provide an excellent model for studying both intraspecific breeding barriers and the regulation of floral organ size and positioning, yet at the molecular level, they are almost completely uncharacterized. In this study, a subtracted cDNA library was generated from developing and mature floral tissues of the thrum morph of Primula vulgaris, subtracted with the same tissues from the pin morph. Differential screening and reverse transcriptase-polymerase chain reaction analysis identified 11 classes of cDNA that were differentially expressed between developing floral morphs. A number of these classes have significant homology to members of gene families implicated in plant development, including rapid alkalinization factors, DExH box RNA helicases, SKS multi-copper oxidases, and AtCHX ion-transporter families, consistent with their potential involvement in the regulation of floral heteromorphy. None of the cDNAs identified appear to be linked to the Primula S-locus suggesting that they are not components of the S-locus itself, and are more likely downstream components of developmental pathways leading to floral heteromorphy.

The molecular biology of self-incompatibility systems in flowering plants

Self-incompatibility is a common mechanism by which flowering plants can exert some control over the process of fertilization. Typically, the self-incompatibility response involves the recognition and rejection of self-incompatible pollen which leads to a block in self-fertilization and, as a consequence, promotes outcrossing. In recent years, considerable progress has been made in the molecular understanding of several self-incompatibility systems. Interestingly, a common mechanism for self-incompatibility is not employed by all flowering plants, but in fact quite diverse mechanisms have been recruited for the rejection of self-incompatible pollen. In this review, the recent advances in the self-incompatibility systems of the Solanaceae, Papaveraceae, and Brassicaceae will be described as well as some of the molecular work that is emerging for the Poaceae and the heteromorphic self-incompatibility systems.

Do homomorphic and heteromorphic self-incompatibility systems have the same sporophytic mechanism?

The view put forward by some authors that flowering plant self-incompatibility mechanisms of the homomorphic sporophytic and heteromorphic sporophytic types have a close evolutionary relationship, with one form being evolved from the other, or both forms directly evolved from ancestors with homomorphic gametophytic incompatibility, is challenged. A review is provided of the various facets of each of the three main self-incompatibility systems, including a detailed summary of our current knowledge of the rejection mechanism, to demonstrate that the implicit assumption that these systems have a common S locus, and also evolutionary theories linking the systems, need to be treated with considerable caution.

Fluctuations in heteromorphic self-incompatibility systems

The genetic determination of heterostyly is briefly reviewed and experimental data are presented on the inheritance of tristyly in Oxalis compressa. It is shown that the model appropriate to Lythrum salicaria, of two diallelic loci, is inadequate to explain segregation patterns found in O. compressa, especially the reversal of dominance of the short phenotype. An extended model having an additional allele at the short locus, and a separate modifier gene, is presented and its deterministic genotype frequency dynamics examined numerically. It is shown that fixation of these extra genes or alleles is unlikely. Problems of testing the extended model are considered.

Studies on heteromorphic self-incompatibility systems: Physiological aspects of the incompatibility system of Primula obconica

In Primula obconica, a species with a heteromorphic self-incompatibility system, the distinction between compatible and incompatible pollen tubes takes place on the stigma surface in thrum flowers, self tubes growing randomly over the papillar cells. No differences were seen between self and cross tube behaviour on the pin stigma surface, but self tubes were inhibited within the stigmatic tissue with differences in tube length evident after 24 h. The stigma surface bears a proteinaceous pellicle and binds the lectin Concanavalin A. Removal of the stigma removes the incompatibility barrier in mature gynoecia. Bud pollination shows that pollen tubes cannot grow in a normal manner on immature stigmas; the random growth of tubes over the stigma surface resembles that of mature thrum selfs. Fewer compatible tubes reach the style base of young gynoecia and smaller numbers of seeds are set than in mature flowers. Pin and thrum pollen grains germinate and grow in aqueous media, thrum tubes growing longer than pin. The presence of H3BO4 and CaCl2 in the growth medium promotes tube elongation and lengths equivalent to compatible styles can be obtained. The pollen grains have proteinaceous materials in their walls which diffuse out on moistening. Prolonged washing in aqueous media removes these materials but the incompatibility reaction remains unchanged. Thus the incompatibility reaction is between pollen tubes and stigmatic tissue and differs from the homomorphic, sporophytic system where pollen wall proteins elicit the incompatibility response.

Studies on heteromorphic selfincompatibility systems: The cytochemistry and ultrastructure of the tapetum of Primula obconica

This paper describes the cytochemistry and ultrastructure of the developing tapetum in Primula obconica, a plant with a heteromorphic, sporophytic self-incompatibility system. The tapetum is of the secretory type and cytochemical tests have shown that when it breaks down proteinaceous (esterase) and lipidic components are deposited on the developing pollen grains. Acid phosphatase, a marker of gametophytic enzyme activity, is confined to the cytoplasm and intine of the developing pollen. Ultrastructural studies show that prior to its dissolution the tapetum undergoes a number of changes. In the early stages of development the tapetum is rich in ribosomes and rough endoplasmic reticulum, but following the breakdown of the tapetal cell wall the main components of the cytoplasm are densely staining spherical bodies surrounded by ribosomes and orbicular bodies, which appear to be confined to the cell periphery. As the cells break down, rod-like fibrils can be seen amongst the degenerate organelles and within the bacular cavities of the pollen. On dehiscence the pollen has a lipidic coating in addition to the fibrillar material in the pollen wall and the remnants of the tapetum can be seen adhering to the fibrous layer of the anther wall. Thus the mature, binucleate pollen of P. obconica is demonstrated to carry wall materials of sporophytic origin.