- Self-incompatibility in plants
Self-incompatibility (SI) is a general name for several genetic mechanisms in
angiosperms, which prevent self-fertilizationand thus encourage outcrossing. In plants with SI, when a pollengrain produced in a plant reaches a stigmaof the same plant or another plant with a similar genotype, the process of pollen germination, pollen tube growth, ovule fertilization, and embryodevelopment is halted at one of its stages, and consequently no seeds are produced. 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.
Mechanisms of self-incompatibility
The best studied mechanisms of SI act by inhibiting the germination of pollen on stigmas, or the elongation of the pollen tube in the styles. These mechanisms are based on
protein-protein interactions, each mechanism being controlled by a single locustermed S, which has many different alleles in the speciespopulation. Despite their similar morphological and genetic manifestations, these mechanisms have evolved independently, and are based on different cellular components;Charlesworth, D., X. Vekemans, V. Castric and S. Glemin (2005). "Plant self-incompatibility systems: a molecular evolutionary perspective." New Phytologist 168: 61–69.] therefore, each mechanism has its own, unique S-locus.
The S-locus contains two basic SI
genes - one expressed in the pistil, and the other in the antherand/or pollen (referred to as the female and male determinants, respectively). Because of their physical proximity, these genes are genetically linked, and are inherited as a unit. Variants of the S-locus are called S-haplotypes. The translation products of the two genes of the S-locus 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 in some species the S-locus contains more than two genes.
Following is a detailed description of the different known mechanisms of SI in plants.
Gametophytic self-incompatibility (GSI)
In gametophytic self-incompatibility (GSI), the SI
phenotypeof 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, Papaveraceaeand Poaceae.Franklin, F. C. H., M. J. Lawrence, and V. E. Franklin-Tong (1995). "Cell and molecular biology of self-incompatibility in flowering plants." Int. Rev. Cytol.158: 1–64.] Two different mechanisms of GSI have been described in detail at the molecular level, and their description follows.
The RNase mechanism
The female component of GSI in the
Solanaceaewas found in 1989.McClure, B. A., V. Haring, , P. R. Ebert, M. A. Anderson, R. J. Simpson, F. Sakiyama, and A. E. Clarke (1989). "Style selfincompatibility gene products of "Nicotiana alata" are ribonucleases." Nature 342: 955–957.] Proteins in the same family were subsequently discovered in the Rosaceaeand Scrophulariaceae. Despite some early doubts about the common ancestry of GSI in these distantly related families, phylogenetic studiesIgic, B., and J. R. Kohn (2001). "Evolutionary relationships among self-incompatibility RNases". Proc. Natl. Acad. Sci. USA 98(23): 13167-71.] and the finding of shared male determinants (F-box proteins)Qiao, H., H. Wang, L. Zhao, J. Zhou, J. Huang, Y. Zhang, and Y. Xue (2004) "The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in "Antirrhinum"." Plant Cell 16(3): 582-95.] Qiao, H., F. Wang, L. Zhao, J. Zhou, Z. Lai, Y. Zhang, T. P. Robbins, and Y. Xue (2004b). "The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility." Plant Cell 16(9): 2307-22.] Ushijima, K., H. Yamane, A. Watari, E. Kakehi, K. Ikeda, N. R. Hauck, A. F. Iezzoni, and R. Tao (2004). "The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of "Prunus avium" and "P. mume"." Plant J. 39(4): 573-86. ] Sijacic, P., X. Wang, A. L. Skirpan, Y. Wang, P. E. Dowd, A. G. McCubbin, S. Huang, and T. Kao (2004). "Identification of the pollen determinant of S-RNase-mediated self-incompatibility." Nature 429: 302-305.] clearly established homology. Consequently, this mechanism arose approximately 90 million years ago, and is the inferred ancestral for approximately 50% of all plants.Igic, B., and J. R. Kohn (2001). "Evolutionary relationships among self-incompatibility RNases". Proc. Natl. Acad. Sci. USA 98(23): 13167-71.] Steinbachs, J. E., and K. E. Holsinger (2002). "S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots." Mol. Biol. Evol. 19(6): 825-9.]
In this mechanism, pollen tube elongation is halted when it has proceeded approximately one third of the way through the style.Franklin-Tong, V. E., and F. C. H. Franklin (2003). "The different mechanisms of gametophytic self-incompatibility." Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358(1434): 1025–1032.] The female component
ribonuclease, termed S-RNase 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.
The male component was only recently identified as the PiSLF protein, a member of the F-box protein group. The members of this group typically function as
ubiquitin ligases; thus, PiSLF might function by targeting heteroallelicS-NRase molecules to proteasomal degradation.
The S-glycoprotein mechanism
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 membranereceptor. 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 concentrationgradient of calcium ions which exists inside the pollen tube, essential for its elongation. [Franklin-Tong, V. E., J. P. Ride, N. D. Read, A. J. Trewawas, and F. C. H. Franklin (1993). "The self-incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium." Plant J. 4: 163–177.] [Franklin-Tong, V. E., G. Hackett, and P. K. Hepler (1997). "Ratioimaging of Ca21 in the self-incompatibility response in pollen tubes of Papaver rhoeas." Plant J. 12: 1375–1386.] [Franklin-Tong, V. E., T. L. Holdaway-Clarke, K. R. Straatman, J. G. Kunkel, and P. K. Hepler (2002). "Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas." Plant J. 29: 333–345.] 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.
cytosolic protein p26, a pyrophosphatase, is inhibited by phosphorylation, [Rudd, J. J., F. C. H. Franklin, J. M. Lord, and V. E. Franklin-Tong (1996). "Increased phosphorylation of a 26-kD pollen protein is induced by the self-incompatibility response in Papaver rhoeas." Plant Cell 8: 713–724.] possibly resulting in arrest of synthesisof molecular building blocks, required for tube elongation. There is depolymerization and reorganization of actinfilaments, within the pollen cytoskeleton. [Geitmann, A., B. N. Snowman, , A. M. C. Emons, and V. E. Franklin-Tong (2000). "Alterations to the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas." Plant Cell 12: 1239–1252.] [Snowman, B. N., D. R. Kovar, G. Shevchenko, V. E. Franklin-Tong, and C. J. Staiger (2002). "Signal-mediated depolymerization of actin in pollen during the self-incompatibility response." Plant Cell 14: 2613–2626.] 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 DNAbegins, [Jordan, N. D., F. C. H. Franklin, and V. E. Franklin-Tong (2000). "Evidence for DNA fragmentation triggered in the selfincompatibility response in pollen of Papaver rhoeas." Plant J. 23: 471–479.] and finally (at 10-14 hours), the cell dies apoptotically. [Thomas, S. G., and V. E. Franklin-Tong (2004). "Self-incompatibility triggers programmed cell death in Papaver pollen." Nature 429: 305-309.]
porophytic 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, Sterculiaceaeand Polemoniaceae. [Goodwillie, C. (1997). "The genetic control of self-incompatibility in Linanthus parviflorus (Polemoniaceae)." Heredity 79: 424–432.] 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.
Dominancerelationships 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 recessiveS allele.Hiscock, S. J., and D. A. Tabah (2003). "The different mechanisms of sporophytic self-incompatibility." Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358(1434): 1037-1045.]
Compared to a population in which all S alleles are co-dominant, the presence of dominance relationships in the population, raises the chances of compatible mating between individuals. 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, D. J. (1974). "Distribution of self-incompatibility alleles and breeding structure of open-pollinated cultivars of Brussels sprouts." Heredity 32: 159–171.]
The SI mechanism in "
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 tapetumtissue, 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 microsporeand pollen (i.e. gametophytically). [Schopfer, C. R., M. E. Nasrallah, and J. B. Nasrallah, (1999). "The male determinant of self-incompatibility in Brassica." Science 266: 1697–1700.] [Takayama, S., H. Shiba, M. Iwano, H. Shimosato, F.-S. Che, N. Kai, M. Watanabe, G. Suzuki, K. Hinata, and A. Isogai (2000). "The pollen determinant of self-incompatibility in Brassica campestris." Proc. Natl Acad. Sci USA 97: 1920–1925.]
The female determinant of the SI response in "Brassica", is a transmembrane protein termed SRK, which has an intracellular
kinasedomain, and a variable extracellular domain. [Stein, J. C., B. Howlett, D. C. Boyes, M. E. Nasrallah, and J. B. Nasrallah (1991). "Molecular cloning of a putative receptor kinase gene encoded by the self-incompatibility locus of Brassica oleracea." Proc. Natl Acad. Sci. USA 88: 8816–8820.] [Nasrallah, J. B., and M. E. Nasrallah (1993). "Pollen–stigma signalling in the sporophytic self-incompatibility response." Pl. Cell 5: 1325–1335.] 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-receptorfor the male determinant, amplifying the SI response. [Takasaki, T., K. Hatakeyama, G. Suzuki, M. Watanabe, A. Isogai, and K. Hinata (2000). "The S receptor kinase determines self-incompatibility in Brassica stigma." Nature 403: 913–916.]
The interaction between the SRK and SCR/SP11 proteins results in
autophosphorylationof the intracellular kinase domain of SRK, [Schopfer, C. R., and J. B. Nasrallah (2000). "Self-incompatibility. Prospects for a novel putative peptide-signaling molecule." Pl. Physiol. 124: 935–939.] [Takayama, S., H. Shimosato, H. Shiba, M. Funato, F.-E. Che, M. Watanabe, M. Iwano, and A. Isogai (2001). "Direct ligand–receptor complex interaction controls Brassica self-incompatibility." Nature 413: 534–538.] and a signal is transmitted into the cell of the stigma. Another protein essential for the SI response is MLPK, a serine- threoninekinase, which is anchored to the plasma membranefrom its intracellular side. [Murase, K., H. Shiba, M. Iwano, F. S. Che, M. Watanabe, A. Isogai, and S. Takayama (2004). "A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling." Science 303(5663): 1516-9.] The downstream cellular and molecular events, leading eventually to pollen inhibition, are poorly described.
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.
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, F. R. (1979). "The biology of heterostyly." New Zealand Journal of Botany 17: 607-635.]
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.
Distylyis determined by a single locus, which has two alleles; tristylyis 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.
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. This restriction maintains a 1:1 ratio between the two genotypes in the population; genotypes are usually randomly scattered in space. [Ornduff, R., and S. G. Weller (1975). "Pattern diversity of incompatibility groups in Jepsonia heterandra (Saxifragaceae)." Evolution 29: 373-5.] [Ganders, F. R. (1976). "Pollen flow in distylous populations of Amsinckia (Boraginaceae)." Canadian Journal of Botany 54: 2530-5.] Tristylous plants contain, in addition to the S locus, the M locus, also with two alleles. The number of possible genotypes is greater here, but a 1:1 ratio exists between individuals of each SI type. [Spieth, P. T. (1971). "A necessary condition for equilibrium in systems exhibiting self-incompatible mating." Theoretical Population Biology 2: 404-18.]
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[Glaettli, M. (2004). Mechanisms involved in the maintenance of inbreeding depression in gynodioecious Silene vulgaris (Caryophyllaceae): an experimental investigation. PhD dissertation, University of Lausanne.] ). 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, A. J. (1956). "Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L." Heredity 10: 257–261.] 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; 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, S. E., and S. J. Mazer (2000). "The absence of cryptic self-incompatibility in Clarkia unguiculata (Onagraceae)." American Journal of Botany 87(2): 191–196.]
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
fruitis set.Seavey, S. F., and K. S. Bawa (1986). "Late-acting self-incompatibility in angiosperms." Botanical Review 52: 195–218.] [Sage, T. L., R. I. Bertin, and E. G. Williams (1994). "Ovarian and other late-acting self-incompatibility systems." In E. G. Williams, R. B. Knox, and A. E. Clarke [eds.] , Genetic control of self-incompatibility and reproductive development in flowering plants, 116–140. Kluwer Academic, Amsterdam.] LSI can be pre-zygotic (e.g. deterioration of the embryo sacprior to pollen tube entry, as in " Narcissus triandrus" [Sage, T. L., F. Strumas, W. W. Cole, and S. C. H. Barrett (1999). "Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae)." American Journal of Botany 86(6): 855–870.] ) or post-zygotic (malformation of the zygoteor embryo, as in certain species of " Asclepias" and in " Spathodea campanulata" [Sage, T. L., and E. G. Williams (1991). "Self-incompatibility in Asclepias." Plant Cell Incomp. Newsl. 23: 55–57.] [Sparrow, F. K., and N. L. Pearson (1948). "Pollen compatibility in Asclepias syriaca." J. Agric. Res. 77: 187–199.] Lipow, S. R., and R. Wyatt (2000). "Single Gene Control of Postzygotic Self-Incompatibility in Poke Milkweed, "Asclepias exaltata" L." Genetics 154: 893–907.] [Bittencourt JR, N. S., P. E. Gibbs, and J. Semir (2003). "Histological study of post-pollination events in Spathodea campanulata Beauv. (Bignoniaceae), a species with late-acting self-incompatibility." Annals of Botany91: 827-834.] ).
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, E. J. (1988). Mutation, Developmental Selection, and Plant Evolution. Columbia University Press, New York.] [Waser N. M., and M. V. Price (1991). "Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped?" American Journal of Botany 78: 1036–1043.] [Nic Lughadha E. (1998). "Preferential outcrossing in Gomidesia (Myrtaceae) is maintained by a post-zygotic mechanism." In: S. J. Owens and P. J. Rudall [eds.] , Reproductive biology in systematics, conservation and economic botany. London: Royal Botanic Gardens, Kew, 363–379.] Supporters, on the other hand, argue for the existence of several basic criteria, which differentiate certain cases of LSI from the inbreeding depression phenomenon.
SI is not universal in flowering plants. Indeed, a great many species are self-compatible (SC). The best estimates indicate that approximately one half of angiosperms are SI. [Igic, B., and J. R. Kohn (2006). "Bias in the studies of outcrossing rate distributions.". Evolution 60: 1098-1103.]
Pollinator decline, variability in pollinator service, and life history traits that are associated with weediness, among other factors, may favor the loss of SI. As a result, mutationsthat break down SI (result in SC) may become common or entirely dominate in natural populations. Similarly, human-mediated artificial selection through selective breedingmay be responsible for the commonly observed self-compatibility in cultivated plants. SC enables more efficient breeding techniques to be employed for crop improvement.
Recent Journal Articles (As of Jan 23, 2006)
* [http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=16159321 Plant self-incompatibility systems: a molecular evolutionary perspective]
* [http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=16120598 Progress in study on signal transduction of gametophytic self-incompatibility]
* [http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=16096969 Gametophyte interaction and sexual reproduction: how plants make a zygote]
* [http://users.rcn.com/jkimball.ma.ultranet/BiologyPages/S/SelfIncompatibilty.html Self-Incompatibility: How Plants Avoid Inbreeding]
* [http://www-biol.paisley.ac.uk/bioref/Genetics/Primula_heterostyly.html Heterostyly in cowslip]
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