Self/non-self discrimination in angiosperm self-incompatibility

Available online at www.sciencedirect.com

Self/non-self discrimination in angiosperm self-incompatibilityMegumi Iwano and Seiji Takayama

Self-incompatibility (SI) in angiosperms prevents inbreeding

and promotes outcrossing to generate genetic diversity. In

many angiosperms, self/non-self recognition in SI is

accomplished by male-specificity and female-specificity

determinants (S-determinants), encoded at the S-locus.

Recent studies using genetic, molecular biological and

biochemical approaches have revealed that angiosperms

utilize diverse self/non-self discrimination systems, which can

be classified into two fundamentally different systems, self-

recognition and non-self recognition systems. The self-

recognition system, adopted by Brassicaceae and

Papaveraceae, depends on a specific interaction between

male and female S-determinants derived from the same S-

haplotype. The non-self recognition system, found in

Solanaceae, depends on non-self (different S-haplotype)-

specific interaction between male and female S-determinants,

and the male S-determinant genes are duplicated to recognize

diverse non-self female S-determinants.

Address

Graduate School of Biological Sciences, Nara Institute of Science and

Technology, 8916-5 Takayama, Ikoma 630-0192, Japan

Corresponding authors: Iwano, Megumi ([email protected]) and

Takayama, Seiji ([email protected])

Current Opinion in Plant Biology 2012, 15:78–83

This review comes from a themed issue on

Growth and Development

Edited by Xuemei Chen and Thomas Laux

Available online 1st October 2011

1369-5266/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2011.09.003

IntroductionAngiosperms have developed self-incompatibility (SI) as

a genetic system to prevent inbreeding and thus promote

outcrossing to generate genetic diversity. SI is based on

the self/non-self discrimination between male and

female. In many angiosperms, SI is controlled by a single

locus, designated S, with multiple haplotypes [1]. Each S-

haplotype encodes both male-specificity and female-

specificity determinants (S-determinants), and the self/

non-self discrimination is accomplished by the S-haplo-

type-specific interaction between these S-determinants.

Classical genetic studies have classified SI into two sys-

tems, gametophytic SI (GSI) and sporophytic SI (SSI),

depending on whether the SI phenotype in pollen is


determined by the S-haplotype of haploid pollen or by

the S-haplotypes of the diploid pollen donor. Recent

molecular analyses have revealed, however, that each

system is not a single system but contains diverged

molecular systems. For example, in GSI, Solanaceae,

Rosaceae and Plantaginaceae use pistil-expressed S-

RNase-based self/non-self recognition system [2–6],

while Papaveraceae use a pollen-expressed transmem-

brane-protein mediated Ca2+ signaling system [7��,8]. In

SSI, Brassicaceae utilizes pistil-expressed receptor kinase

for self/non-self recognition [9], while such an S-locus

associated receptor kinase has not been found in Con-

volvulaceae [10] and Asteraceae [11]. Thus, this classifi-

cation of GSI and SSI does not reflect the similarity of

mechanisms, but probably reflects whether male S-deter-

minant is produced in haploid pollen or in diploid anther.

Recent intense studies using molecular and biochemical

approaches have revealed that self/non-self discrimi-

nation mechanisms in SI can be classified into two fun-

damentally different systems, self-recognition and non-

self recognition. In this review, we focus on the self-

recognition systems in Brassicaceae and Papaveraceae,

and the non-self-recognition system in Solanaceae, and

compare these with the self/non-self recognition systems

in other organisms. As we only focus on the recognition

part of SI systems, other reviews should be consulted for

details about the downstream SI signaling pathway lead-

ing to self-pollen rejection [8,12–15].

Self-recognition systemSelf-recognition SI, adopted by Brassicaceae and Papa-

veraceae, depends on a specific interaction between

male-determinants and female-determinants derived

from the same S-haplotype. These determinant genes

are tightly linked in the S-locus and suggested to have co-

evolved, keeping the recognition specificities between

two determinants.

SI in BrassicaceaeIn Brassicaceae, the S-locus encodes two highly poly-

morphic proteins: S-locus receptor kinase (SRK), and S-

locus protein 11 (SP11, or S-locus cysteine-rich protein,

SCR). SRK is a membrane-spanning Ser/Thr receptor

kinase that localizes to the plasma membrane of stigmatic

papilla cells and functions as the female S-determinant

[16]. SP11 is a small basic protein secreted from the

anther tapetum and localizes to the pollen coat [17–19]. SP11 is a ligand of SRK and functions as the male

S-determinant [20,21]. SRK and SP11 genes are tightly

linked and inherited like a single Mendelian locus gene.

This tight genetic linkage provides the basis for self-

recognition in each S-haplotype.

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http://dx.doi.org/10.1016/j.pbi.2011.09.003

Angiosperm self-incompatibility Iwano and Takayama 79

The self-recognition, i.e. the S-haplotype specific inter-

action between SP11 and its cognate SRK, has been

shown by a series of biochemical studies. A binding

experiment using 125I-labeled-S8-SP11 suggested that it

strongly binds to the stigmatic membrane of S8-haplotype

(Kd = 0.7 nM) but not of the S9-haplotype [20]. Cross-

linking and immunological analyses suggested that 125I-

labeled-S8-SP11 directly binds to S8-SRK and a 60-kDa

protein in the stigmatic membrane of S8-haplotype

[20,22]. Affinity purification and LC–MS/MS analysis

of SP11-binding stigmatic proteins have revealed that

the 60-kDa protein is a truncated form of SRK (tSRK)

containing the extracellular, transmembrane and part

of the intracellular juxtamembrane domains [23��].Although the stigmatic extract contains a soluble form

of extracellular domain of SRK (eSRK), which is pro-

duced by alternative splicing [24], it exhibited no high-

affinity binding to SP11. Interestingly, an artificially

expressed dimerized form of eSRK exhibited high affinity

binding to SP11 [23��]. Another recent study suggested

that two regions in the extracellular domain of SRK

mediated the homo-dimerization of eSRK [25]. Taken

together, these studies suggested that SRK on the

stigmatic membrane is in an equilibrium between the

inactive monomeric or dimeric low-affinity forms and

the dimeric active high-affinity form, and that the SP11

binding to its cognate SRK stabilizes its dimeric active

form, which is expected to trigger the SI responses in the

papilla cell [13,23��] (Figure 1).

Figure 1

Female S-determinant Male S-determinant

SRK SP11/SCR

SRK

SP11/SCR

PM of papilla cell

Papilla cell cytoplasm

Cell wall

S1 haplotype

S2 haplotype

P P

Current Opinion in Plant Biology

Self-recognition SI system in Brassicaceae. The S-locus encodes female

and male S-determinants, designated SRK and SP11 (or SCR),

respectively. In self-pollination, the self (same S-haplotype)-specific

SP11 binding to its cognate SRK stabilizes SRK in an active dimeric form

on plasma membrane (PM), which triggers SI responses in the stigmatic

papilla cell.


In self-recognition SI, the male and the female S-deter-

minant genes must be tightly linked in the S-locus and

their products must maintain interaction in each S-hap-

lotype. Evolutionary changes are necessary in both genes,

since any mutation affecting only one gene would result

in a nonfunctional S-haplotype. Probably reflecting these

requirements, SRK and SP11 genes in Brassicaceae show

patterns of co-evolution [26,27]. However, the molecular

process allowing the evolution of new S-haplotypes

remains controversial.

SI in PapaveraceaeIn the field poppy Papaver rhoeas, SI is gametophytically

controlled and the incompatible reaction occurs in the

pollen grain, in contrast to that in Brassicaceae, which

occurs in the stigmatic papilla cell. The female S-deter-

minant, PrsS (P. rhoeas stile S), is a highly polymorphic

(40–46% divergence between alleles) small (�15 kDa)

protein secreted by the stigmatic papilla cells [8]. The

self-recognition mode of SI was clearly shown by an invitro bioassay using recombinant PrsS protein expressed

in Escherichia coli. The recombinant PrsS triggers a series

of SI responses, including increase in cytosolic free Ca2+

and depolymerization of the actin cytoskeleton, resulting

in pollen inhibition and programmed cell death, only

when it was applied to the self-pollen (with same S-

haplotype) but not to the cross-pollen [8,28].

Genomic sequence analysis of the S1-locus identified the

pollen-S gene, PrpS (P. rhoeas pollen S), which was

located within 0.5 kb from PrsS. PrpS is a novel �20-

kDa transmembrane protein, with 3–5 predicted trans-

membrane helices [7��]. Examination of the PrsS and

PrpS sequences suggested that these alleles have co-

evolved and are likely to be similarly ancient. Knockdown

of PrpS by adding its antisense oligonucleotide in the

abovementioned in vitro bioassay system rescued the

pollen from PrsS-induced growth inhibition, suggesting

that PrpS is the male S-determinant. Furthermore, a 15-

amino-acid peptide corresponding to part of the predicted

extracellular loop segment of PrpS was shown to interact

with PrsS, and the addition of this peptide into the

bioassay system also alleviated PrsS-induced pollen inhi-

bition. These results suggested that the direct self-recog-

nition between PrpS and PrsS triggers the SI responses in

the pollen tube [7��] (Figure 2).

A similar SI system has been identified in a hermaphro-

ditic solitary ascidian, Ciona intestinalis [29��]. SI in C.intestinalis is gametophytically controlled by the haploid

genotype of the male-gametophyte (sperm) and incom-

patible reaction occurs in the male-gametophyte as for

Papaveraceae SI. This SI system is controlled by two

unlinked genetic loci (A and B), and so, in this sense, this

system might be more like that of grasses, which is

controlled by two SI loci (S and Z) [30]. Positional cloning

of A and B loci of C. intestinalis revealed that both loci had


80 Growth and Development

Figure 2

Female S-determinant

Ca2+?

Male S-determinant

S1 haplotype

S2 haplotype

PrsS PrpS

PrsS

PrpS PM of pollen tube

Pollen cytoplasm

Pistil


Self-recognition SI system in Papaveraceae. The S-locus encodes

female and male S-determinants, designated PrsS and PrpS,

respectively. In self-pollination, the self (same S-haplotype)-specific

PrsS binding to its cognate PrpS on pollen plasma membrane (PM)

elicits Ca2+ influx in the pollen tube, which triggers SI responses leading

to programmed cell death.

no overall synteny but commonly contained a tightly

linked pair of genes, s-Themis and v-Themis, each v-Themislocated within the long first intron of respective s-Themis[29��]. v-Themis is a fibrinogen-like ligand locating on

the vitelline coat of the egg, and s-Themis is a transmem-

brane polycystin receptor, which spans the sperm plasma

membrane five or eleven times and contains a cation

channel domain. Therefore, the interaction between v-

Themis and s-Themis is expected to induce the elevation

of cytoplasmic cations (e.g. Ca2+) in the male-gameto-

phyte as in the case of Papaveraceae SI, although the

direct interaction between these determinants and the

following SI responses need to be validated in future.

Non-self recognition systemAnother completely different SI mechanism is non-self

recognition SI, which involves the recognition of non-self

partners and disregard of the self partner. This type of

self/non-self discrimination has been known in the mat-

ing type selection in lower eukaryotes, for example, fungi

and mushrooms [31–33]. Recently, such a non-self recog-

nition system has been demonstrated in plants of the

Solanaceae.

SI in SolanaceaeSI in Solanaceae, Rosaceae and Plantaginaceae families

is controlled by the haploid genotype of pollen and the

SI response occurs in the pollen tube. The female S-

determinant in these families is the style glycoproteins


of �30-kDa, S-RNase, possessing ribonuclease activity

[2,3]. If the S-haplotype of pollen matches one of the two

S-haplotypes of the style, S-RNase exerts cytotoxicity

inside the self-pollen tube to inhibit its growth. The

male S-determinant was firstly identified as an F-box

protein, named S-locus F-box (SLF or SFB), which was

predicted to be a component of an SCF (Skp1–Cullin1–F-box) complex [4–6]. Based on the molecular nature of

these S-determinants, a protein degradation model has

been proposed [9,34,35]. This is a non-self recognition

model and predicts that an SLF allelic variant specifi-

cally recognizes its non-self S-RNases and mediates

their degradation by the ubiquitin–26S-proteasome sys-

tem. However, SLF shows much lower allelic sequence

diversity than S-RNase, and it was puzzling how an SLFallelic product could recognize a large repertoire of

highly divergent non-self S-RNases to allow cross-com-

patible pollinations. Moreover, phylogenetic studies of

SLF and S-RNase in Solanaceae and Plantaginaceae

showed no evidence of co-evolution, with SLF having

a much shorter evolutionary history [36]. Furthermore,

two distinct S-haplotypes (S7 and S19) in Petunia have

been shown to carry 100% identical SLF, although the

amino acid sequences of their S-RNases are 45% iden-

tical [37��]. These findings suggested that firstly ident-

ified SLF is not the sole element of the male S-

determinant.

A thorough search of the pollen transcriptome in Petuniarevealed that multiple SLF and SLF-like genes (desig-

nated SLFs) were specifically expressed in pollen [37��].These SLFs were classified into six subgroups, and all

exhibited amino-acid sequence polymorphisms among

S-haplotypes and genetic linkage to the S-locus. Trans-

formation experiments showed that at least three types

of SLFs function as the male S-determinant; each SLFcaused breakdown of SI when it was expressed in pollen

of a subset of non-self S-haplotypes. Furthermore,

immunoprecipitation experiments using pollen expres-

sing FLAG-tagged SLF revealed that each SLF specifi-

cally interacts with non-self S-RNases of a subset of S-

haplotypes such that each SLF caused breakdown of SI.

Based on these results, a ‘collaborative non-self recog-

nition’ model was proposed [37��] (Figure 3). In this

model, the male S-determinant comprises multiple

types of SLFs. Within an S-haplotype, the product of

each type of SLF interacts with a subset of non-self S-

RNases, and the products of multiple types, including

yet uncharacterized ones, are required for the entire

suite of non-self S-RNases to be collectively recognized

and detoxified. In ‘collaborative non-self recognition’

SI, increasing the repertoire of SLFs would be advan-

tageous, as this would increase the number of potential

mating partners. Other SI species in Solanaceae, Rosa-

ceae, and Plantaginaceae also have a single S-RNase and

multiple SLFs in the S-loci [38–40]. Whether these

other species also adopt similar ‘collaborative non-self



Figure 3

Female S-determinant Male S-determinant

S1 haplotype

S2 haplotype

S-RNase SLF/SFB

S-RNase

SLF/SFB

RNA

PM of Pollen tube

Pollen cytoplasm

Pistil


Non-self recognition SI system in Solanaceae. The S-locus encodes a

single female and multiple male S-determinants, designated S-RNase

and SLFs, respectively. In self-pollination, none of SLFs interacts with

self S-RNase (derived from the same S-haplotype), which breaks down

pollen RNA to inhibit its growth. In cross-pollination, some members of

SLFs interact with non-self S-RNase (derived from a different S-

haplotype), which detoxifies S-RNase thus allowing pollen tube growth.

recognition’ SI, and how these multiple types of SLFgenes have emerged in the S-locus should be important

questions to be addressed in future.

Non-self recognition has been reported in mating recog-

nition in basidiomycete fungi [31–33]. For mating to occur

in basidiomycetes, compatible mates must have different

haplotypes at two unlinked mating type loci, A and B. The

A locus encodes two homeodomain transcription factors,

whereas the B locus encodes one pheromone receptor and

multiple pheromones. Pheromones encoded by one Blocus only interact with receptors of different alleles. In

this manner, each receptor interacts with multiple phero-

mones and each pheromone interacts with multiple recep-

tors. In addition, to maintain stable dikaryon, two

homeodomain transcription factors encoded in the A locus

must form active heterodimers, which can be achieved only

when they are derived from different alleles. In these non-

self recognition systems, interacting recognition molecules

must eliminate self-reactivity, while maintaining broad

reactivity with non-self. Comparative analysis of these

mating type loci and plant S-loci may provide important

clues as to how these complicated loci have evolved.

ConclusionsSI in the angiosperms is known for at least 71 families and

has been recorded in more than 250 of the 600 genera [41].

The presence of a high proportion of selfing species is also

known, and major selfing species are thought to have


evolved through the loss of SI [42]. Recent molecular

approaches combined with evolutionary approaches have

also revealed part of the history of selfing.

Arabidopsis thaliana is a self-compatible selfing species in

the genus Arabidopsis of the Brassicaceae, derived from an

obligate outbreeding ancestor by loss of SI. Introduction

of functional SCR and SRK gene pairs isolated from self-

incompatible Arabidopsis lyrata or Capsella grandiflora into

some accessions of A. thaliana could confer stable SI

responses [43–45]. Furthermore, recent comparative gen-

ome analysis revealed that 95% of European accessions

possess a disruptive mutation in the SCR gene (i.e. a 213-

bp inversion or its derivative haplotypes with deletions),

while some accessions, including Wei-1, still retain a

functional SRK gene [46,47��]. When the 213-bp inver-

sion in SCR was inverted and expressed in Wei-1, the

transformant restored the SI response. These results

suggested that the inversion within SCR is the primary

mutation disrupting SI, which was spread and fixed in a

wide range of European A. thaliana populations.

Selfing is disadvantageous when selfed offspring store

recessive traits, but it may nevertheless be needed for

reproductive assurance under environments where polli-

nators or mates are scarce, as first proposed by Charles

Darwin [48]. In fact, angiosperm families in which SI is

found also contain significant proportions of self-compa-

tible species. The two states are commonly interspersed

within clades, implying frequent evolutionary transitions

[49]. A more recent study suggested, however, that in the

Solanaceae family, species with SI diversify at a signifi-

cantly higher rate than those without it [50�]. The appar-

ent short-term advantages of potentially self-compatible

individuals are therefore offset by strong species selec-

tion, which favors obligate outcrossing. Considering this

together with the fact that there are at least three and

probably more diversified self/non-self recognition sys-

tems in SI, angiosperms must have repeatedly lost and re-

acquired SI systems in the course of their evolution.

AcknowledgementsThis work is supported by Grant-in-Aid for Scientific Research onInnovative Areas (21112003 to M.I.; 23113001, 23113002 to S.T.) and byGrants-in-Aid for Scientific Research (23570056 to M.I.; 21248014 to S.T.)from the Ministry of Education, Culture, Sports, Science and Technology ofJapan (MEXT).

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http://dx.doi.org/10.1093/aob/mcq253

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http://dx.doi.org/10.1104/pp.111.174912

http://dx.doi.org/10.1104/pp.111.174912


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Self/non-self discrimination in angiosperm self-incompatibility