Self-incompatibility in plants

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Self-incompatibility (SI) is one of the most important means to prevent selfing and promote the generation of new genotypes in plants, and it is considered as one of the causes for the spread and success of the angiosperms, on our planet.

SI is a general name for several physiological mechanisms in angiosperms, which are designed to prevent reproduction which is based on self-fertilization and mating between relatives, and encourage the outcrossing of individuals with differing genotypes. In plants with SI, when a pollen grain produced in a plant reaches a stigma of the same plant or another plant with a similar genotype, the process of pollen germination, pollen tube growth, ovule fertilization, and embryo development is halted at one of its stages, and consequently no seeds are produced. Although other mechanisms that prevent self-fertilization have evolved (dichogamy, herkogamy, dioecy), they tend to either fail to prevent self-fertilization among flowers of the same plant (geitonogamy), or dramatically reduce reproductive efficiency.

Self-incompatibility is not universal in flowering plants. Indeed, a great many species are self-compatible. Pollinator decline, variability in pollinator service, and life history traits that are associated with weediness, among other factors, may favor the loss of self-incompatibility. As a result, mutations that break down self-incompatibility (result in self-compatibility) may become common or entirely dominate in natural populations. Similarly, human-mediated artificial selection through selective breeding may be responsible for the commonly observed self-compatibility in cultivated plants. Self-compatibility enables more efficient breeding techniques to be employed for crop improvement.

Flowering plants are often hermaphrodites and have perfect flowers. That is, both male (anther) and female (pistil) reproductive organs are in close proximity within a flower. The stigma or style can recognize and reject a plant's own pollen or pollen from related individuals (sharing as little as one allele).

1 Mechanisms of Self-Incompatibility
2 References
3 See also
4 Recent Journal Articles (As of Jan 23, 2006)
5 External links

[edit] Mechanisms of Self-Incompatibility

The most abundant and studied mechanisms of SI, act by inhibiting the germination of pollen on stigmas, or the elongation of the pollen tube. These mechanisms are based on protein-protein interactions, and are governed by a single locus termed S, which has many different alleles in the species population. Despite their similar morphological and genetic manifestations, these mechanisms have evolved independently, and are based on different cellular components (Charlesworth et al. 2005).

The S locus contains two basic SI genes - one expressed in the pistil, and the other in the anther and/or pollen (referred to as the female and male determinants, respectively). Because of their physical proximity, these genes are genetically linked, and are regarded as a single allele. The translation products of the two genes from the same allele, are two proteins which, by interacting with one another, lead to the arrest of pollen germination and/or pollen tube elongation, and thereby generate an SI response, preventing fertilization. However, when a female determinant interacts with a male determinant of a different allele, no SI is created, and fertilization ensues. This is a simplistic description of the general mechanism of SI, which is more complicated, and usually dependant on more than one allele.

Following is a detailed description of the different known mechanisms of SI in plants.

[edit] Gametophytic Self-Incompatibility (GSI)

In gametophytic self-incompatibility (GSI), the SI phenotype of the pollen is determined by its own gametophytic haploid genotype. This is the more common type of SI, existing in the families: Solanaceae, Rosaceae, Scrophulariaceae, Fabaceae, Onagraceae, Campanulaceae, Papaveraceae and Poaceae (Franklin et al. 1995). Two different mechanisms of GSI have been described in detail at the molecular level, and their description follows.

[edit] The RNase mechanism

The female component of GSI in the Solanaceae was found in 1989 (McClure et al. 1989). Proteins in the same family were subsequently discovered in the Rosaceae and Scrophulariaceae. Despite some early doubts about the common ancestry of GSI in these distantly related families, phylogenetic studies (Igic and Kohn 2001) and the finding of shared male determinants (F-box proteins; Qiao et al. 2004, Ushijima et al. 2004, Sijacic et al. 2004) clearly established homology. Consequently, this mechanism arose approximately 90 million years ago, and is the inferred ancestral for approximately 50% of all plants (Igic and Kohn 2001, Steinbachs and Holsinger 2002).

In this mechanism, pollen tube elongation is halted when it has proceeded approximately one third of the way through the style (Franklin-Tong and Franklin 2003). The female component ribonuclease, termed S-RNase (McClure et al. 1989) probably causes degradation of the ribosomal RNA (rRNA) inside the pollen tube, in the case of identical male and female S alleles, and consequently pollen tube elongation is arrested, and the pollen grain dies (Franklin-Tong and Franklin 2003).

The male component was only recently identified as the PiSLF protein, a member of the F-box protein group (Sijacic et al. 2004). The members of this group typically function as ubiquitin ligases; thus, PiSLF might function by targeting heteroallelic S-NRase molecules to proteasomal degradation.

[edit] The S-glycoprotein Mechanism

The following mechanism was described in detail in Papaver rhoeas. In this mechanism, pollen growth is inhibited within minutes of its placement on the stigma (Franklin-Tong and Franklin 2003).

The female determinant is a small, extracellular molecule, expressed in the stigma; the identity of the male determinant remains elusive, but it is probably some cell membrane receptor (Franklin-Tong and Franklin 2003). The interaction between male and female determinants transmits a cellular signal into the pollen tube, resulting in strong influx of calcium cations; this interferes with the intracellular concentration gradient of calcium ions which exists inside the pollen tube, essential for its elongation (Franklin-Tong et al. 1993, 1997, 2002). The influx of calcium ions arrests tube elongation within 1-2 minutes. At this stage, pollen inhibition is still reversible, and elongation can be resumed by applying certain manipulations, resulting in ovule fertilization (Franklin-Tong and Franklin 2003).

Subsequently, the cytosolic protein p26, a pyrophosphatase, is inhibited by phosphorylation (Rudd et al. 1996), possibly resulting in arrest of synthesis of molecular building blocks, required for tube elongation. There is depolymerization and reorganization of actin filaments, within the pollen cytoskeleton (Geitmann et al. 2000; Snowman et al. 2002). Within 10 minutes from the placement on the stigma, the pollen is committed to a process which ends in its death. At 3-4 hours past pollination, fragmentation of pollen DNA begins (Jordan et al. 2000), and finally (at 10-14 hours), the cell dies apoptotically (Franklin-Tong and Franklin 2003; Thomas and Franklin-Tong 2004).

[edit] Sporophytic Self-Incompatibility (SSI)

In sporophytic self-incompatibility (SSI), the SI phenotype of the pollen is determined by the diploid genotype of the anther (the sporophyte) in which it was created. This form of SI was identified in the families: Brassicaceae, Asteraceae, Convolvulaceae, Betulaceae, Caryophyllaceae, Sterculiaceae and Polemoniaceae (Goodwillie 1997). Up to this day, only one mechanism of SSI has been described in detail at the molecular level, in Brassica (Brassicaceae).

Since SSI is determined by a diploid genotype, the pollen and pistil each express the translation products of two different alleles, i.e. two male and two female determinants. Dominance relationships often exist between pairs of alleles, resulting in complicated patterns of compatibility/self-incompatibility. These dominance relationships also allow the generation of individuals homozygous for a recessive S allele (Hiscock and Tabah 2003).

Compared to a population in which al S alleles are co-dominant, the presence of dominance relationships in the population, raises the chances of compatible mating between individuals (Hiscock and Tabah 2003). The frequency ratio between recessive and dominant S alleles, reflects a dynamic balance between reproduction assurance (favoured by recessive alleles) and avoidance of selfing (favoured by dominant alleles) (Ockendon 1974).

[edit] The SI Mechanism in Brassica

As previously mentioned, the SI phenotype of the pollen is determined by the diploid genotype of the anther. In Brassica, the pollen coat, derived from the anther's tapetum tissue, carries the translation products of the two S alleles. These are small, cysteine-rich proteins. The gene encoding these proteins is termed SCR or SP11, and is expressed in the anther tapetum (i.e. sporophytically), as well as in the microspore and pollen (i.e. gametophytically) (Schopfer et al. 1999; Takayama et al. 2000).

The female determinant of the SI response in Brassica, is a transmembrane protein termed SRK, which has an intracellular kinase domain, and a variable extracellular domain (Stein et al. 1991; Nasrallah and Nasrallah 1993). SRK is expressed in the stigma, and probably functions as a receptor for the SCR/SP11 protein in the pollen coat. Another stigmatic protein, termed SLG, is highly similar in sequence to the SRK protein, and seems to function as a co-receptor for the male determinant, amplifying the SI response (Takasaki et al. 2000).

The interaction between the SRK and SCR/SP11 proteins results in autophosphorylation of the intracellular kinase domain of SRK (chopfer and Nasrallah 2000; Takayama et al. 2001), and a signal is transmitted into the papilla cell of the stigma. Another protein essential for the SI response is MLPK, a serine-threonine kinase, which is anchored to the plasma membrane from its intracellular side (Murase et al. 2004). The downstream cellular and molecular events, leading eventually to pollen inhibition, are poorly described.

[edit] Other Mechanisms of Self-Incompatibility

These mechanisms are less abundant and have received only limited attention in scientific research. Therefore, they are still poorly understood.

[edit] Heteromorphic Self-Incompatibility

A distinct SI mechanism exists in heterostylous flowers, termed heteromorphic self-incompatibility. This mechanism is probably not evolutionarily related to the more familiar mechanisms, which are differentially defined as homomorphic self-incompatibility (Ganders 1979).

Almost all heterostylous taxa feature SI to some extent. The loci responsible for SI in heterostylous flowers, are strongly linked to the loci responsible for flower polymorphism, and these traits are inherited together, in a single allele. Distyly is determined by a single locus, which has two alleles; tristyly is determined by two loci, each with two alleles. Heteromorphic SI is sporophytic, i.e. both alleles in the male plant, determine the SI response in the pollen. SI loci always contain only two alleles in the population, one of which is dominant over the other, in both pollen and pistil. Variance in SI alleles parallels the variance in flower morphs, thus pollen from one morph can fertilize only pistils from the other morph. In tristylous flowers, each flower contains two types of stamens; each stamen produces pollen capable of fertilizing only one flower morph, out of the three existing morphs (Ganders 1979).

A population of a distylous plant contains only two SI genotypes: ss and Ss. Fertilization is possible only between genotypes; each genotype cannot fertilize itself (Ganders 1979). This restriction maintains a 1:1 ratio between the two genotypes in the population; genotypes are usually randomly scattered in space (Ornduff and Weller 1975; Ganders 1976). Tristylous plants contain, in addition to the S locus, the M locus, also with two alleles (Ganders 1979). The number of possible genotypes is greater here, but a 1:1 ratio exists between individuals of each SI type (Spieth 1971).

[edit] Cryptic Self-Incompatibility (CSI)

Cryptic self-incompatibility (CSI) exists in a limited number of taxa (for example, there is evidence for CSI in Silene vulgaris, Caryophyllaceae - Glaetlli 2004). In this mechanism, the simultaneous presence of cross and self pollen on the same stigma, results in higher seed set from cross pollen, relative to self pollen (Bateman 1956). However, as opposed to 'complete' or 'absolute' SI, in CSI, self-pollination without the presence of competing cross pollen, results in successive fertilization and seed set (Bateman 1956); in this way, reproduction is assured, even in the absence of cross-pollination. CSI acts, at least in some species, at the stage of pollen tube elongation, and leads to faster elongation of cross pollen tubes, relative to self pollen tubes. The cellular and molecular mechanisms of CSI have not been described.

The strength of a CSI response can be defined, as the ratio of crossed to selfed ovules, formed when equal amounts of cross and self pollen, are placed upon the stigma; in the taxa described up to this day, this ratio ranges between 3.2 and 11.5 (Travers and Mazer 2000).

[edit] Late-Acting Self-Incompatibility (LSI)

Late-acting self-incompatibility (LSI) is also termed ovarian self-incompatibility (OSI). In this mechanism, self pollen germinates and reaches the ovules, but no fruit is set (Seavey and Bawa 1986; Sage et al. 1994). LSI can be pre-zygotic (e.g. deterioration of the embryo sac prior to pollen tube entry, as in Narcissus triandrus - Sage et al. 1999) or post-zygotic (malformation of the zygote or embryo, as in certain species of Asclepias and in Spathodea campanulata - Sparrow and Pearson 1948; Sage and Williams 1991; Lipow and Wyatt 2000; Bittencourt et al. 2003).

The existence of the LSI mechanism among different taxa and in general, is subject for scientific debate. Criticizers claim, that absence of fruit set is due to genetic defects (homozygosity for lethal recessive alleles), which are the direct result of self-fertilization (inbreeding depression) (Klekowski 1988; Waser and Price 1991; Nic Lughadha 1998). Supporters, on the other hand, argue for the existence of several basic criteria, which differentiate certain cases of LSI from the inbreeding depression phenomenon (Seavey and Bawa 1986; Lipow and Wyatt 2000).

[edit] References

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