Self-Incompatibility: How Plants Avoid Inbreeding

• Evolution seems to favor (and be favored by) genetic variability.
• Genetic variability is promoted by outbreeding: sexual reproduction between genetically dissimilar parents.
• (Just why sexual reproduction is so popular throughout the world of living things is still a hotly-debated question, but the fact remains.)

• anthers producing pollen (the source of the male gametes) and
• the pistil producing the egg (the female gamete),

  Link to a discussion of sexual reproduction in angiosperms.

A variety of solutions have been tried in the plant kingdom.

• Having imperfect flowers; that is, flowers that are either male or female.
  • Dioecy. The imperfect flowers are present on separate plants. Dioecy is the equivalent of the separate sexes of most animals. But it is rather rare. Some examples:
    • poplars
    • hollies
  • Monoecy. The imperfect flowers are present on the same plant. But if they mature at different times, self-fertilization is avoided. Corn (maize) is a common example.

• Heteromorphic flowers.

  The flowers are perfect but come in two structural types; for example

  1. long stamens with a short style and
  2. short stamens with a long style.

  A single plant has one type or the other.

  If the pollinator has a short tongue, pollination is favored from the first type to the second - but not the reverse.

  Heteromorphic flowers are not common, and even in the angiosperm families that favor them (e.g., primroses, flax), the same biochemical mechanisms of self-incompatibility that we will find (below) in homomorphic flowers are usually present as well.

• Homomorphic flowers. All flowers have exactly the same structure. Avoidance of self-fertilization depends on genetic/biochemical mechanisms. There are two quite different types of self-incompatibility.
  • Sporophytic self-incompatibility (SSI)
  • Gametophytic self-incompatibility (GSI)

Sporophytic Self-Incompatibility (SSI)

This form of self-incompatibility has been studied intensively in members of the mustard family (Brassica), including turnips, rape, cabbage, broccoli, and cauliflower.

• Rejection of self pollen is controlled by the diploid genotype of the sporophyte generation.
• The control lies in the "S-locus", which is actually a cluster of three tightly-linked loci:
  • SLG (S-Locus Glycoprotein) which encodes part of a receptor present in the cell wall of the stigma;
  • SRK (S-Receptor Kinase), which encodes the other part of the receptor. Kinases attach phosphate groups to other proteins. SRK is transmembrane protein embedded in the plasma membrane of the stigma cell.
  • SCR (S-locus Cysteine-Rich protein), which encodes a soluble, secreted ligand for the same receptor.
• Because the plants cannot fertilize themselves, they tend to be heterozygous; that is, carry a pair of different S loci (here designated S₁ and S₂).
• However, dozens of different S alleles may be present in the population of the species; that is; the S-locus in the species is extremely polymorphic (analogous to the major histocompatibility locus of vertebrates — Link).
• The difference between the alleles is concentrated in certain "hypervariable regions" of the receptor (analogous to the hypervariable regions that provide the great binding diversity of antibodies — Link).

• Pollen will not germinate on the stigma (diploid) of a flower that contains either of the two alleles in the sporophyte parent that produced the pollen.
• This holds true even though each pollen grain — being haploid — contains only one of the alleles.
• In the example shown here, the S₂ pollen, which was produced by a S₁S₂ parent, cannot germinate on an S₁S₃ stigma.

• The S₁S₂ pollen-producing sporophyte synthesizes both SCR₁ and SCR₂ for incorporation in (and later release from) both S₁ and S₂ pollen grains.
• If either SCR molecule can bind to either receptor on the pistil, the kinase triggers a series of events that lead to failure of the stigma to support germination of the pollen grain. Among these events is the ubiquination of proteins targeting them for destruction in proteasomes.
• If this path is not triggered (e.g., pollen from an S₁S₂ parent on an S₃S₄ stigma, the pollen germinates successfully.

Gametophytic Self-Incompatibility (GSI)

• the Solanaceae (potatoes, tomatoes, and tobacco)
• beets (Beta vulgaris)
• buttercups (Ranunculus)
• lilies
• roses
• many grasses

• The S loci are (as in SSI plants) extremely polymorphic; that is, there is an abundance of multiple alleles in the population.
• Incompatibility is controlled by the single S allele in the haploid pollen grain.
• Thus a pollen grain will grow in any pistil that does not contain the same allele (so, as shown here and in contrast to what happens in SSI, S₂ pollen from an S₁S₂ parent will grow down an S₁S₃ style.

• All pollen grains — incompatible as well as compatible — germinate forming pollen tubes that begin to grow down the style.
• However, growth of incompatible pollen tubes stops in the style while compatible tubes go on to fertilize the egg in the ovary.
• The block within incompatible pollen tubes is created by an S-locus-encoded ribonuclease (RNase), which is
  • synthesized within the style;
  • enters the pollen tube and
  • destroys its RNA molecules
  • halting pollen tube growth.
• The RNase molecules contain a hypervariable region which is the basis for each S specificity (S₁, S₂, S₃, etc.).
• The pollen tube expresses a molecule that targets RNase for destruction (in proteasomes). This targeting molecule also exists is different S specificities (S₁, S₂, S₃, etc.).
• In compatible ("nonself") tubes, the targeting molecule can do its job — thus permitting RNA to survive and growth to continue.
• How the targeting molecule is prevented from acting in incompatibile ("self") tubes is still under investigation. Perhaps the binding of, for example, the S₁ targeting molecule to an S₁ binding site on the S₁ RNase prevents destruction of the RNase and so the RNAs of the pollen tube are destroyed and growth is halted.