Self Incompatibility 2012 Inroads

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166 Vol. 1, No. 2, July-December 2012

Molecular Perspective to Understand the Phenomenon of Self-Incompatibilityand Its Utilisation in Crop Plants

Gulzar S. Sanghera1*, Waseem Hussian2, Gurpreet Singh3 and G .A. Parray4

1Senior Scientist (PBG),2Research Scholar (PBG), SKUAST-Kashmir, Mountain Research Centre for Field Crops, Khudwani, Anantnag-192102,J&K, India3Research Associate (PBG), School of Agricultural Biotechnology, PAU, Ludhiana-141001, India4Associate Director Research, SKUAST-Kashmir, Mountain Research Centre for Field Crops, Khudwani, Anantnag-192102, J&K, India

ABSTRACT

Self-incompatibility (SI) is a genetically controlled mechanism for rejection of own pollen. It has been a favourite topic for botanistsand geneticists since Darwin, who first discussed this phenomenon and suggested its central significance during the evolution offlowering plants. Different genetic and mechanistic systems of SI among different plant families suggest either multiple origins of SIor considerable evolutionary diversification. Within the last two decades, molecular and biochemical analyses have significantlycontributed to the elucidation of the complex series of interactions occurring at the pollen–stigma interface. Molecular analyses ofSI systems have focused on identifying and characterising the pollen and pistil components of the self-incompatible response as wellas other proteins and events that lead to pollen rejection. In this review, an attempt has been made to provide a comprehensive insightfor the molecular dissection of this important mechanism for its utilisation in crop improvement.

Keywords: Self-incompatibility, S-allele, pollen–stigma interaction, molecular analysis

INTRODUCTIONMany bisexual flowering plants avoid the deleterious effectsof inbreeding by employing genetically controlled self-incompatibility (SI) mechanisms to ensure out crossing(Charlesworth and Charlesworth, 1987). SI mechanismsprovide the biochemical machinery necessary for plants torecognise and reject their own pollen as well as non-self-pollen with a genotype sufficiently similar to elicit activationof the SI mechanism. SI plays an important role in shapingthe spatial and temporal distribution of genetic diversity inplant populations and is believed to influence patterns oflineage diversification in clades within which thesemechanisms are utilised (Igic et al., 2008). Approximately96% of flowering plants produce perfect flowers that containboth the male and female reproductive organs in closeproximity; consequently, they would have a strong tendency

to self-fertilise if there were no mechanisms to prevent themfrom doing so. As inbreeding can result in reduced fitnessin the progeny, hermaphroditic plants have adopted variousreproductive strategies, including SI, by which inbreedingis prevented and outcrosses are promoted (de Nettancourt,2001). SI allows the pistil of a flower to distinguish betweengenetically related (self) and unrelated (non-self) pollen.This self/non-self-recognition results in the inhibition ofgermination of self-pollen on the stigmatic surface or inthe inhibition of growth of self-pollen tubes in the style. SI,thus the most sophisticated and widespread in occurrence,has been known in flowering plants for over a century sinceDarwin’s description in 1876 (Darwin, 1876). SI wasdefined by de Nettancourt (1977) as ‘the inability of a fertilehermaphrodite seed plant to produce zygotes after self-pollination’. In other words, SI forms a pre-zygotic

INROADSVol. 1, No. 2, July - December 2012

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reproductive barrier by which incompatible pollen/pollentubes are prevented from delivering sperm cells to the ovaryto affect double fertilisation (Sims, 1993; Charlesworth etal., 2005). Incompatibility is widespread and present in thespecies of Leguminosae, Solanaceae, Cruciferae,Compositae and Gramineae. In cultivated crops,incompatibility is found in red clover, aliska clover, whiteclover, alfalfa, tall fescue, ryegrass, rye, sugarbeets,sunflower, pearmillet, tobacco, potatoes, bahigrass,bermudagrass and others (Haring et al., 1990; deNettancourt, 2001; Allen and Hiscock, 2008). Identificationof the biochemical components of SI mechanisms hasproven to be difficult in most lineages (Clarke andNewbigin, 1993). Within the last two decades, scientistshave been able to complement Darwin’s geneticobservations with molecular and biochemical analyses,which have significantly contributed to the elucidation ofthe complex series of interactions occurring at the pollen–stigma interface (Takasaki et al., 2000; Silva and Goring,2001; Franklin-Tong and Franklin, 2003). Molecularanalyses of SI systems have focused on identifying andcharacterising the pollen and pistil components of the self-incompatible response as well as other proteins, and eventsthat lead to pollen rejection are discussed hereafter.

Incompatibility SystemsSI systems may be classified into two basic types:heteromorphic and homomorphic.

(1) Heteromorphic incompatibility: In heteromorphicincompatibility, flowers of the same species can have twoor three different morphological forms, and successfulpollination occurs only between flowers of differentmorphological forms (Darwin, 1876; Haldane, 1933). Thisis caused by differences in the lengths of stamens and style(called heterostyly) and may be of two types: (1) distylicand (2) tristylic. In the distylic forms (e.g., Fagopyrum sp.,Pulmmaria sp., Linus sp., Potigorum sp.), two types of floralstructure (short style and high anther, long style and shortanther) are found (Figure 1). In one flower type called thepin, the styles are long while the anthers are short. In theother flower type, thrum, the reverse is true (e.g., inPrimula). The pin trait is conditioned by the genotype ss,while thrum is conditioned by the genotype Ss. A cross ofpin (ss) × pin (ss), as well as thrum (Ss) × thrum (Ss) is

incompatible. However, pin (ss) × thrum (Ss) or vice versais compatible. In tristylic types (e.g., Lythrum sp., Oxalissp.), the population comprises three distinct groupscharacterised by long-, mid- and short-styled flowers, witheach flower-bearing anther at two different heights, whichdo not correspond to the level of the stigma (Li et al., 2007).

Figure 1: Heteromorphic incompatibility showing floralmodifications in which anthers and pistils are of different lengthsin different plants. Long- and short-styled primrose flowers(showing pollinations that are compatible) and the three geneshypothesised to control style length, pollen incompatibility typeand anther position. This type of incompatibility is believed to bealways of the sporophytic type. Pin and thrum flowers occur inflowers such as Primula, Forsythia, Oxalis and Silia.

Figure 2: Homomorphic self-incompatibility (SI). Gametophyticcontrol of pollen incompatibility types is shown; the haploid pollengrains express the allele they carry. This system is known inSolanaceae, Papaveraceae, Rosaceae and Antirrhinum species (inan unrelated angiosperm family, Plantaginaceae). In other families,pollen specificities are controlled by the genotype of the diploidanther tissue (sporophytic system). This is known in Brassicaceaeand in Ipomoea, in the family Convolvulaceae.

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(2) Homomorphic incompatibility: There are two kindsof homomorphic incompatibility – gametophytic andsporophytic (Figure 2) depending on the genetic control ofthe pollen behaviour during SI interactions. In many cases,SI is controlled by a single multi-allelic locus, the S locus;however, complementary multiple-locus systems also exist.

Gametophytic self-incompatibility (GSI)This type of incompatibility is found in clovers, grasses,sugarbeets, potatoes and tobacco. In gametophyticincompatibility (originally called the oppositional factorsystem as the incompatibility allele in the style opposes thepenetration of pollen tubes with the same allele), the abilityof the pollen to function is determined by its own genotypeand not by the plant that produces it. The rate of pollen tubegrowth is controlled by a series of multiple alleles, which aredesignated S1, S2, S3 and so on. The pollen is rejected whenthe S haplotype of the haploid pollen matches either of thetwo S haplotypes of the diploid pistil (Figure 3). Unlikesporophytic systems, there is no dominance of S alleles instyle; both operate to oppose the growth of the respectivepollen tube. The co-dominance in style prevents any self-pollination and leads invariably to heterozygote progeny.

Genetics of GSIGSI is controlled by a single polyallelic S locus. The geneticsof the incompatibility system based on the one-locus systemfound in tobacco and clovers has been already describedabove (Figure 3). The number of incompatibility alleleswithin species may be rather large, so that cross-pollinationsoccur freely. More than 100 S alleles in Trifolium pretense,41 in red clover and at least 64 alleles in white clover havebeen estimated in these populations. More complex systemsare also known, e.g., two polyallelic loci in grassesdesignated as S & Z (Figure 4); three and four loci each inRanunculus ascaris and Beta vulgaris, respectively(Lundqvist et al., 1973; Igic et al., 2003).

Sporophytic system incompatibility (SSI)This system is found in sunflower, cabbage, broccoli, cacao,buckwheat and other species. In sporophytic incompatibility,the incompatibility characteristics of the pollen are determinedby the plant (sporophyte) that produces it, and thus dominanceinteractions between S alleles are possible. When both pollenand stigma S alleles are co-dominant, the pollen is recognised

as self and rejected if either of the two S haplotypes of itsparent matches one of the two S haplotypes of the pistil (Liet al., 2007, 2011). The incompatible pollen may be inhibitedon the stigma surface. For example, a plant with genotypeS1S2 where S1 is dominant to S2 will produce pollen that willfunction like S1. Furthermore, the S1 pollen will be rejectedby an S1 style but received by an S2 style. Hence, homozygotesof S alleles are possible. However, interactions of S allelescan occur independently for pollen and stigma, leading tocomplicated compatibility/incompatibility patterns anddifferences in reciprocal compatibility.

Figure 3: The gametophytic system of SI showing the pollen tubegrowth, in compatible and incompatible pollinations. In the firstone, pollen tubes do not grow in styles carrying similar alleles forincompatibility (S1S2 x S1S2). In the second one, only pollen grainswith different incompatibility alleles from those in the style developnormal pollen tubes (S1S3 x S1S2). In third one, all pollen grainscarry different incompatibility alleles from those in the styles anddevelop normal pollen tubes (S1S2 x S3S4).

Figure 4: Genetic control of gametophytic self-incompatibility(GSI) by two multiple-allelic loci S and Z. When both pollen Sand Z alleles are matched in the pistil, incompatibility occurs, andpollen growth is inhibited. Otherwise, pollen is compatible. Thedegree of compatibility can be 0, 50, 75 and 100% compatible,depending on the genotypes of pollen and stigma. Reciprocalcrosses (marked with ‘*’) between plants of the genotypes S1S2Z1Z2and S1S2Z1Z2 produce pollen of different proportions of compatiblepollen. If a S1S1Z1Z2 genotype is the pollen donor and crossed withS1S1Z1Z2 genotype pistils, the pollen is incompatible, while if aS1S2Z1Z2 genotype is the pollen donor and pollinated on S1S1Z1Z2pistils, 50% of the pollen is compatible.

Molecular Perspective to Understand the Phenomenon of Self-Incompatibility and Its Utilisation in Crop Plants

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The sporophytic system of incompatibility differs from thegametophytic system in that S alleles exhibit dominance,the dominance being determined by the plant producingthe pollen, and hindrance to pollen germination or pollentube growth is localised on the surface of the stigma incontrast to the gametophytic system in which the hindranceto pollen tube growth is in the style. Furthermore, in thesporophytic system, plants may be produced that arehomozygous for an S allele either by passing the SI barrieror through pseudo-SI. This feature has been utilised in theproduction of hybrids in self-incompatible species.

Incompatibility is expressed in one of three general ways,depending on the species. The germination of the pollenmay be decreased (e.g., in broccoli). Sometimes, removingthe stigma allows normal pollen germination. In the secondway, pollen germination is normal, but pollen tube growthis inhibited in the style (e.g., tobacco). In the third scenario,the incompatibility reaction occurs after fertilisation (e.g.,in Gesteria). This third mechanism is rare.

Si PathwaysIt is expected that the amino acid stretches between thecysteine residues, varying in length and compositionbetween SCR alleles to form loops at the surface of thefolded protein. By imparting extensive structural diversityon small SCR polypeptide molecules, such loops couldmediate specificity in the SI recognition reaction.

Having established that the SCR gene determines pollen SIspecificity, it is suggested that the SCR gene productrepresents the pollen-borne ligand postulated to activate thestigmatic SRK receptor. The small hydrophilic polypeptidepredicted by the SCR sequence is expected to localise tothe pollen coat after its secretion from developingmicrospores (similar to the secretion of othergametophytically expressed components of the pollen coat(Doughty et al., 1998) and also possibly from cells of thetapetum. In either case, SCR molecules would mix readilywithin the anther locule and consequently, the pollen coatof all pollen grains in an S-locus heterozygote wouldincorporate the SCR protein encoded by each of the twoparental S haplotypes, as predicted by sporophytic controlof SI in Brassica (SI in the sporophytic system, the pollenphenotype in S-locus heterozygotes is determined by thetwo S alleles carried by the diploid parent plant and not by

the single S allele carried by the haploid pollen grain). SCRwould translocate into the cell walls of the stigma epidermalcell through the pollen coat–stigma contact zone.

A stigma cell is capable of discriminating between twopollen grains, one self and one cross, placed touching eachother on its surface. The cross grain will germinate andpenetrate the style tissues within 40 minutes, whereas theself-pollen barely begins to germinate (Dickinson, 1995).Self-pollen rejection requires protein synthesis in the stigma(Sarker et al., 1988), and can be overcome by creation ofhigh humidity, which stimulates rapid pollen germination.Analysis of self-incompatible mutants suggests that the self-pollen rejection mechanism may involve the participationof a specific aquaporin (water transport channel) (Ikeda etal., 1997).

Stone et al. (1999) investigated the stigma protein thatinteracts with the kinase domain of SRK, one of the threecandidate protein ARCI (a protein that binds to the SRKkinase domain) became phosphorylated on the binding SRK(Gu et al., 1998). Encouragingly, ARCI is expressed in thestigma, but until now, evidence for its involvement in SIhas been circumstantial. These investigators report the useof antisense oligonucleotides to block the expression ofARCI in Brassica. Strikingly, both pollination and seed setstudies showed that the SI system broke down in plantsthat did not express ARCI, confirming ARCI as a keycomponent of the self-pollen rejection response. Of course,the manner by which the activation of ARCI is linked tothe interruption of stigma’s water supply to the pollen grainsremains to be determined and SI mechanisms occur in someof species with dry stigma also.

Molecular Basis of SiSince the beginning of the 1980s, the rapid expansion ofnew techniques in molecular biology and protein chemistry,and their use to study SI systems, has allowed significantadvances in our knowledge of which molecules are involvedin male–female recognition in flowering plants. Four of thefamilies that display GSI, namely Solanaceae, Rosaceae,Scrophulariaceae and Papaveraceae, and one of thefamilies that exhibit soporophytic SI (SSI), Brassicaceae,have been extensively studied at the molecular level. Thesefamilies often contain plant species of substantial interestfor horticulture or agriculture, and thus, have been the object

Gulzar S Sanghera, Waseem Hussian, Gurpreet Singh and G A Parray

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of intense classical genetic work in the past. For all thesefive families, SI is controlled by a single polymorphic Slocus. During the past two decades, much progress has beenmade in identifying and characterising the S-locus genesthat control the specificity of the SI interaction in the fivefamilies mentioned above. Comparisons of the S-locusgenes expressed in the pistil among the different familieshave revealed three biochemically distinct mechanisms. TheSolanaceae, Rosaceae and Scrophulariaceae use the samemechanism, the Papaveraceae uses another and theBrassicaceae uses a third. For the Solanaceae andPapaveraceae mechanisms, the gene that controls femalespecificity has been identified; these genes were named theS-RNase gene and the S-gene, respectively. The Solanaceaemechanism involves S-RNase-mediated degradation ofRNA in self-pollen tubes. The Papaveraceae mechanismis mediated by a signal transduction cascade in pollen thatinvolves a number of known components of signaltransduction (e.g., Ca2+, phosphoinositides, protein kinasesand phosphatases). For the SSI mechanism found in theBrassicaceae, both the gene that controls male specificity,S-locus cysteine-rich protein (SCR)/S-locus protein-11(SP11), and the gene that controls female specificity, S-locus receptor kinase (SRK), have been identified. The SIresponse is mediated via a signal transduction cascade inthe stigmatic papilla, which is elicited by the interaction ofa pollen-borne ligand, SCR/SP11, and SRK, a receptorkinase in the stigmatic papilla (Table-1). GSI is employedby a number of families; however, only a few have been

studied at the molecular level. The most extensively studiedfamilies are the Solanaceae, Rosaceae, Scrophulariaceaeand Papaveraceae. In most families, GSI is controlled by asingle locus (S locus, termed after the word ‘sterility’) withmultiple alleles. However, there are more complex systemsinvolving several gene loci, e.g., some grass species havetwo loci (Lundqvist, 1956) or Beta vulgaris has four loci(Larsen, 1977). SSI is not as widespread as GSI and islargely studied in the Brassicaceae and Asteraceae. Variousmechanisms providing an insight into the molecular basisof SI are briefly described below.

Model for the S-Rnase-Dependent Mechanism ofGSIIn GSI, the phenotype of the pollen is determined by itsown haploid genotype. In the Rosaceae family, GSI iscontrolled by the single, polymorphic S locus. Fertilisationis prevented when the S allele expressed by the haploidpollen grain matches one of the S alleles expressed in thepistil. Pollen grains from the S1S2 anther are incompatiblewith the S1S2 pistil. If two different cultivars have identicalS genotypes, it presents an incompatible combination ineach direction (Kozma et al., 2003; Nyéki and Szabó, 1995).These cultivars are mutually self-incompatible, i.e., in otherterms, cross- or inter-incompatible. The first report aboutRNases in plant style described that their activity variedgreatly among species (Schrauwen and Linskens, 1972). Adiscovery, which gave further background for the hypothesis

Plant Type Genetic Female MaleFamily of SI Locus Determinant Determinant Mechanism ReferencesSolanaceae,Rosaceae, GSI S-locus RNase SLF/SFB? RNase–mediated VieiraScrophulariaceae degradation of et al., 2007

pollen tube RNAPapaveraceae GSI S-locus S-gene Unknown S- Protein–mediated Franklin-

signaling cascade Tong (2007)in pollen

Brassicaceae SSI S-locus SRK SCR/SP11 Receptor-kinase– Sherman-Broylesmediated signaling and Nasrallahin stigma (2008)

Table-1: A scheme of the S locus and a list of the identified female and male determinant genes. The S locus contains at least two genes,one encoding the male determinant that is carried by the pollen grain, and the other encoding the female determinant that is expressedin the pistil. Both the male and female determinants are polymorphic and inherited as one segregating unit. The variants of this genecomplex are called S haplotypes. The recognition of self/non-self-operates at the level of the protein–protein interactions between thetwo determinants, and an incompatible response occurs when both determinants are issued from the same S haplotype. Thus far, bothdeterminants have been identified in the Brassicaceae and Solanaceae.


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that RNases may have more diverse functions in plants,was made in 1989 by Clarke’s and team at the Universityof Melbourne (McClure et al., 1989). They were the firstwho clarified that the basic S-glycoproteins associated withGSI in Nicotiana alata possessed inherent ribonucleaseactivity. The stylar S-glycoproteins can penetrate the pollentube and degrade RNA in the cytoplasm. This wouldinterfere with protein synthesis; however, no in vivoevidence has been known to support this hypothesis. Half ayear later, the same laboratory presented the adequate proof(McClure et al., 1990): it was revealed by the use of the32P isotope that ribosomal RNAs from styles of compatiblecrosses are intact, but degraded in incompatible crosses.The Solanaceae, Rosaceae and Scrophulariaceae familiesall share a female S-determinant, an S-RNase and an F-boxprotein, suggesting the involvement of RNA and proteindegradation in the system (Kao and Tsukamoto, 2004;Franklin-Tong and Franklin, 2003). The S-RNase was firstidentified in the Solanaceae and thus referred to as S-RNase-mediated type of SI as Solanaceae type SI. The Solanaceae-type SI is under gametophytic control (GSI), and rejectionof self-pollen occurs during pollen tube growth in the style.S-RNase is the sole female factor determining the S-haplotype specificity of the pistil. The conclusive evidencethat SLF/SFB (S-haplotype-specific F-box) that encodes thepollen S-determinant was finally obtained fromtransformation experiments in Petunia inflata (Sijacic etal., 2004). One plausible model that represents themechanism of this type is the ‘inhibitor model’, in whichthe pollen S-determinant was postulated to be an inhibitorthat could inhibit all S-RNases with the exception of thecognate S-RNase (Kao and McCubbin, 1996). Thus, oncein the pollen tube cytosol, S-RNases sharing no S-allelespecificity with the pollen S-locus F-box (SLF) protein willinteract with a general pollen RNase inhibitor thatinactivates the S-RNases. By contrast, if the S-RNase andSLF share the same S-allele specificity (here S1), the generalpollen RNase inhibitor will not be able to inactivate theself S1-RNase. The mechanisms of S-haplotype-specificpollen inhibition are presented diagrammatically (Figure5). Several cDNA cloning, sequencing or genomic PCR-based experiments were carried out in case of several Salleles from more and more rosaceous species, includingJapanese pear (Sassa and Hirano, 1997), apple (Kitaharaand Matsumoto, 2002), almond (López et al., 2004), sweetcherry (Sonneveld et al., 2003), sour cherry (Hauck et al.,

2002) and apricot (Halász et al., 2005). The increasingabundance of data confirmed the rosaceous S-RNase genestructure being completely identical (Kubo et al., 2010).

Figure 5: Molecular model of the self-incompatibility response inthe Solanaceae, Rosaceae and Scrophulariaceae. The S locusconsists of two genes, S-RNase and SLF/SFB. S-RNase is the femaledeterminant and is secreted in large amounts into the extracellularmatrix of the style. In a pollinated style, S-RNase is incorporatedinto the pollen tubes and functions as a cytotoxin that degradespollen RNA. Although the S-RNase enters the pollen tubesregardless of their S-haplotypes, RNA degradation occurs only inself-pollen tubes. SLF/SFB is the male determinant and is amember of the F-box family of proteins, which generally functionas a component of an E3–ubiquitin ligase complex. Thus, SLF/SFB is expected to be involved in ubiquitin-mediated proteindegradation of non-self-S-RNases.

However, this has also several unclear details, and furtherbiochemical investigations are required to shed light on themechanism of S-RNase inactivation and the precise role ofSFB in protecting self-S-RNases from degradation.

Model for the S-Glucoprotein-DependentMechanism of GSI System InPapaver rhoeasSI in the field poppy, P. rhoeas is also under gametophyticcontrol (GSI) in that the S phenotype of pollen is determinedby its haploid S genotype. However, the identified S protein(female determinant) and the mechanisms involved in polleninhibition differ dramatically from those in the Solanaceae.In the Papaveraceae, the only identified female determinantinduces a Ca2+-dependent signalling network that ultimatelyresults in the death of incompatible pollen (Lane andLawrence, 1993). SI involves the recognition and rejectionof self- or incompatible pollen by the pistil. In P. rhoeas, SIuses a Ca2+-based signalling cascade triggered by the S


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pollination in Papaver (Bosch and Franklin-Tong 2008). Theresult of programmed cell death is an irreversible rejectionof the self-incompatible pollen (Thomas and Franklin-Tong,2004).

The recent identification of the pollen S protein as the Slocus F-box (SLF) protein fits nicely with this model (Sijacicet al., 2004, Bosch and Franklin-Tong, 2008). F boxes aremembers of larger protein complexes, the SCF complexes,which are also involved in targeting proteins for degradationby the proteasome. One can speculate that SLF may fit intothe inhibitor model by mediating the degradation of all non-self S-RNases, and therefore allow the continued growthof compatible pollen tubes. Following a self-incompatiblepollination, an allelic match between SLF and S-RNasewould somehow prevent the degradation of S-RNase (Kuboet al., 2010), and pollen tube growth would be arrested bythe degradation of pollen RNA. P. rhoeas possesses a GSIsystem not homologous to any other SI mechanismcharacterised at the molecular level. Four previouslypublished full-length stigmatic S alleles from the genusPapaver exhibited remarkable sequence divergence, butthese studies failed to amplify additional S alleles despitecrossing evidence for more than 60 S alleles in P. rhoeasalone (Paape et al., 2011).

Model for the SRK-Dependent Mechanism of SSIinBrassicaceae The various naturally occurring, classicallydefined S alleles that have been described in Brassicahave been arranged in a dominance series based on theirgenetic behaviour relative to other alleles in heterozygousplants (Thomson and Taylor, 1966). A classical geneticanalysis has grouped the Brassica S alleles into twocategories based on their phenotypic effect on SIcharacteristics. The first group of alleles (high-activity)is placed relatively high on the dominance scale andexhibit a strong self-incompatible phenotype in whichan average of 0-10 pollen tubes develop per self-pollinated stigma. The second group of alleles (low-activity) demonstrates a weak or leaky self-incompatiblephenotypic effect in which 10-30 pollen tubes developper self-pollinated stigma and they are considered to berecessive (Nasrallah et al., 1991). Molecular analysis of

protein, which is encoded by the stigmatic component ofthe S locus. This results in the rapid inhibition ofincompatible pollen tube growth (Franklin-Tong et al.,2002). The possible mechanism is representeddiagrammatically below (Figure 6). The Papaveraceae SIsystem also involves signalling pathways which are,however, quite different from the Brassica system. A smallligand-like S protein has been found to be secreted bystigmatic cells at the top of the pistil. The stigmatic S proteinis believed to bind to an unidentified pollen S receptor toinitiate signalling inside the pollen. Several signalling eventshave been observed including a rapid increase in Ca2+ levels,protein phosphorylation and depolymerisation of the actincytoskeleton resulting in growth arrest of the self-pollen(Franklin-Tong and Franklin, 2003). Recently, programmedcell death has also been identified as the definitive contributorin this rejection response. The key features of programmedcell death, including nuclear DNA fragmentation, leakageof cytochrome c from the mitochondria and cleavage of poly(ADP-ribose) polymerase, were all observed during self-

Figure 6: Molecular model of self-incompatibility response in thePapaveraceae. Only the female determinant gene has beenidentified, which encodes a secreted stigma protein named Sprotein. The S protein interacts with the assumed S-haplotype-specific pollen receptor (the putative male determinant) andinduces Ca2+ influx in the shank of the pollen tube. SBP is anintegral proteoglycan of the pollen plasma membranes and isexpected to function as an accessory receptor. Ca2+ influx stimulatesincreases in [Ca2+], with some contribution from both intracellularand extracellular sources. These increases in [Ca2+], trigger thedownstream signalling cascades, which that result in rapid growthinhibition and ultimately in the death of incompatible pollen tubes.


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the S-locus region shows that this locus is a complexlocus spanning many kilobases and containing severalphysically linked transcriptional units that co-segregateperfectly with the SI phenotype (Boyes et al., 1997,Casselman et al., 2000; Hiscock and McInnis, 2003). Asubset of genes within the S-locus complex (‘Shaplotype’) is highly polymorphic as expected for genesinvolved in recognition, and specific combinations ofallelic forms of each of these genes are believed to definedifferent SI specificities. Thus, the S locus may be viewedas a master recognition locus that encodes the function(s)required for the stigma to distinguish self-related fromself-unrelated pollen.

The SI in the Brassicaceae belongs to SSI and, so far, is theonly SSI system in which the mechanism has beencharacterised at the molecular level (Kachroo et al. 2002;Hiscock and McInnis, 2003). Arabidopsis halleri and A.lyrata are two Brassicaceae species with functionalsporophytic SI (Schierup et al., 2001; Llaurens et al., 2008),which diverged ~2 Ma (Koch and Matschinger, 2007; Castricand Vekemans, 2007). Two genes have been identified asessential for determination of incompatibility mating typesin the Brassicaceae: S-receptor kinase (SRK; Stein et al.,1991) and S-locus protein 11/S locus cystein-rich protein(SP11/SCR, hereafter referred to as SCR; Schopfer et al.,1999; Suzuki et al., 1999). The female determinant, SRK, isexpressed in the stigma as a transmembrane receptor kinase,which recognises the gene product of SCR (the maledeterminant) located on the pollen surface. Recognition ofself-SCR by SRK receptors leads to haplotype-specificrejection of self-pollen (Kachroo et al., 2002; Sherman-Broyles and Nasrallah, 2008). The SRK and SCR genes aretypically inherited as a single unit, as a recombination betweenthe two determinant genes would disrupt the SI response(Uyenoyama et al., 2000). The possible mechanism isrepresented diagrammatically (Figure 7). Despite recentprogress in our understanding of the molecular basis of flowerdevelopment and plant SI systems, the molecular mechanismsunderlying heteromorphic SI remain unresolved. Byexamining differentially expressed genes from the styles ofthe two floral morphs, Yasui et al., (2012) recently identifieda gene that is expressed only in short-styled plants. The novelgene identified was completely linked to the S locus in alinkage analysis of 1,373 plants and had homology to EARLY

FLOWERING 3. They named this gene as S-LOCUS EARLYFLOWERING 3 (S-ELF3).

Figure 8: Application of self-incompatibility in practical plantbreeding. Sporophytic incompatibility is widely used in breedingof cabbage and other Brassica species. Single-cross hybrids aremore uniform and easier to produce. The top cross is commonlyused. A single self-incompatible parent is used as female, and isopen pollinated by a desirable cultivar as the pollen source.

downstream of SRK has not yet been characterised, but theessential positive effectors include MLPK and ARC1.MLPK localises the papilla cell membrane and may form asignalling complex with SRK. ARC1, an E3 ubiquitin ligase,binds to the kinase domain of SRK in a phosphorylation-dependent manner and may target unknown substrates for

Figure 7: Molecular model of the self-incompatibility (SI) responsein the Brassicaceae, The S locus consists of three genes, SRK, SP11and SLG. The SRK receptor kinase is the female determinant andspans the plasma membrane of the stigma papilla cell. SP11 is themale determinant and is predominantly expressed in the anthertapetum and accumulates in the pollen coat during pollenmaturation. Upon pollination, SP11 penetrates the papilla cell walland binds SRK in an S-haplotype-specific manner.

This binding induces the autophosphorylation of SRK,triggering a signalling cascade that results in the rejectionof self-pollen. SLG is not essential for the self-/non-selfrecognition but localises in the papilla cell wall and enhancesthe SI reaction in some S haplotypes. The signalling cascade


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ubiquitination. The proteasomal degradation of thesesubstrates could result in pollen rejection.

Plant Breeding Implications of SIInfertility of any kind hinders plant breeding. However, thishandicap may be used as a tool to facilitate breeding bycertain methods. SI may be temporarily overcome bytechniques or strategies, such as removal of the stigmasurface (or application of electric shock), early pollination(before inhibitory proteins form) or lowering thetemperature (to slow down the development of the inhibitorysubstance). SI promotes heterozygosity. Consequently,selfing self-incompatible plants can create significantvariability from which a breeder can select superiorrecombinants. SI may be used in plant breeding (for F1hybrids, synthetics, triploids), but first homozygous linesmust be developed. SI systems for hybrid seed productionhave been established for certain crops (e.g., cabbage, kale),which exhibit sporophytic incompatibility (Figure 8).Inbred lines (compatible inbreds) are used as parents. Thesesystems are generally used to manage pollinations forcommercial production of hybrid seeds. Gametophyticincompatibility occurs in vegetatively propagated species.The clones to be hybridised are planted in adjacent rows.

Breakdown of SIThere are a number of factors and environmentalcircumstances, which in most species can preventincompatibility reaction to occur or enable theincompatible pollen tube to escape the pistil barrier andaccomplish self-pollination. Such factors are of importancefor breeders engaged in the production of hybrids basedon SI. The effects these factors can induce may perhapscorrespond to: (1) inhibition of S-gene action, (2)inactivation of S-gene products and (3) transmission ofgrowth stimulus enabling the incompatible pollen tube toeffect fertilisation before floral abscission, although anumber of factors/environmental conditions result in thebreakdown of SI (de Nettancourt, 1977). These may bebud pollination, high or low temperatures, use of storedpollen, end-of-season effects, high relative humidity,irradiation of styles, hormone treatment of pollen or pistils,increased CO2 content, application of NaCl, doublepollination, use of pollen mixtures, treatment of stigmawith ether soluble pollen coat material, very early and late

flower pollination, mechanical methods such as steel brushor cotton pad rub stigma and then pollination, electricallyaided and thermally aided pollination, clipping of the styleand then pollination fertilisation in vitro. The effectivenessof these methods depend on the nature of S alleles, geneticbackground, the age and vigour of plant and flower, typeof crop and the incompatibility system. Mutagens (agentsof mutation) such as X-rays, radioactive sources such asP32, and certain chemicals have been used to make a self-infertile genotype self-fertile. Such a change is easier toachieve in gametophytic systems than in sporophyticsystems. Furthermore, the effect of incompatibility allelesin gametophytic incompatibility is not so great as toprohibit self-fertilisation entirely; for most species, anoccasional seed may set from pollen carrying the sameallele that is present in the stylar tissue. This condition isreferred to as pseudo-self-compatibility. In addition, self-fertility alleles (Sf) may be present, which render the allelesfor incompatibility ineffective. The Sf allele is a part ofthe S-allele series and may arise by mutation from an Sallele. Sometimes, incompatible diploid species becomeself-compatible with induction of polyploidy, yet somepolyploidy species, like white clover, possess alleles forSI.

CONCLUSIONSDespite a number of setbacks and encounters withunexpected complexities, a picture is starting to emerge ofhow rejection of self-pollen is mediated at the molecularlevel, at least on the female side. However, several questionsremain to be answered, the most important being the natureof the male component of the SI response. On pollen–stigmainteractions, several groups described their ongoing effortsto identify the male component using approaches rangingfrom differential screening, to mutagenic approaches andchromosome walking at the S locus, to biochemicalapproaches and bioassays. One important aspect of the SIresponse, about which very little is known, is the mechanismof self-pollen rejection, following recognition by the stigma.Some recent advances in this area have been describedabove. Many other questions will become easier to addressas we learn more about how SI works at the molecular level.An obvious example is the molecular basis of dominancebetween S haplotypes. The evidence that SRK moleculesassociate with each other in an oligomeric complex suggests


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a possible mechanism for dominance in stigmas. Currentresearch aimed at understanding the molecular mechanismof SI builds on genetic and physiological studies that havebeen carried out over the past few decades. This reviewprovided an exciting forum to discuss the recentdevelopments in this area. Further analysis of the recognitionreaction of SI will be conducted through a combination ofa broad spectrum of approaches, including genetics,genomics, molecular biology, biochemistry and biophysics.Although a large amount of information is now known abouteach of the different SI systems, many pieces of the puzzlesare still missing. All three known molecular mechanismsthat plants have adopted to prevent inbreeding differ greatlywith the only commonality between the S RNase andBrassica SRK systems being the employment of ubiquitin-mediated protein degradation. Recent findings havefurthered our understanding of these systems, but it will beexciting to follow how these stories continue to unfold, andto see what new systems will be uncovered as other self-incompatible plant families are studied.

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