Self-incompatibility systems: barriers to self-fertilization in flowering plants

Flowering plants (angiosperms) are the most prevalent and evolutionarily advanced group of plants. Success of these plants is owed to several unique evolutionary adaptations that aid in reproduction: the flower, the closed carpel, double fertilization, and the ultimate products of fertilization, seeds enclosed in the fruit. Angiosperms exhibit a vast array of reproductive strategies, including both asexual and sexual, the latter of which includes both self-fertilization and cross-fertilization. Asexual reproduction and self-fertilization are important reproductive strategies in a variety of situations, such as when mates are scarce or when the environment remains relatively stable. However, reproductive strategies promoting cross-fertilization are critical to angiosperm success, since they contribute to the creation of genetically diverse populations, which increase the probability that at least one individual in a population will survive given changing environmental conditions. The evolution of several physical and genetic barriers to self-fertilization or fertilization among closely related individuals is thus widespread in angiosperms. A major genetic barrier to self-fertilization is self-incompatibility (SI), which allows female reproductive cells to discriminate between "self" and "non-self" pollen, and specifically reject self pollen. Evidence for the importance of SI in angiosperm evolution lies in the highly diverse set of mechanisms used by various angiosperm families for recognition of self pollen tube development and preventing self-fertilization.     

不同社会等级雄性根田鼠对自身和同性陌生气味的辨别

采用两两遭遇法确定雄性根田鼠的社会等级,然后以新鲜尿作气味源,在行为选择箱中观察不同社会等级雄性根田鼠对自身气味和非自身气味的行为响应模式,结果表明:种群中从属个体对自身尿液存在明显偏好,其对自身尿液的接近潜伏期显著短于非自身尿液,而访问时间、自我修饰频次都显著高于非自身尿液;种群中优势个体则优先访问非自身尿液,其对非自身尿液的访问时间、嗅舔时间、自我修饰及反标记均显著高于自身尿液;对非自身尿液,不同社会等级雄性个体之间存在明显不同的行为反应模式。这说明,不同社会等级雄性根田鼠具有自我识别的能力且模式不同,同时其对非自身尿气味响应模式的差异也与自身的社会等级有关。     

The Papaver self-incompatibility pollen S-determinant, PrpS, functions in Arabidopsis thaliana

Many angiosperms use specific interactions between pollen and pistil proteins as "self" recognition and/or rejection mechanisms to prevent self-fertilization. Self-incompatibility (SI) is encoded by a multiallelic S locus, comprising pollen and pistil S-determinants. In Papaver rhoeas, cognate pistil and pollen S-determinants, PrpS, a pollen-expressed transmembrane protein, and PrsS, a pistil-expressed secreted protein, interact to trigger a Ca(2+)-dependent signaling network, resulting in inhibition of pollen tube growth, cytoskeletal alterations, and programmed cell death (PCD) in incompatible pollen. We introduced the PrpS gene into Arabidopsis thaliana, a self-compatible model plant. Exposing transgenic A. thaliana pollen to recombinant Papaver PrsS protein triggered remarkably similar responses to those observed in incompatible Papaver pollen: S-specific inhibition and hallmark features of Papaver SI. Our findings demonstrate that Papaver PrpS is functional in a species with no SI system that diverged ~140 million years ago. This suggests that the Papaver SI system uses cellular targets that are, perhaps, common to all eudicots and that endogenous signaling components can be recruited to elicit a response that most likely never operated in this species. This will be of interest to biologists interested in the evolution of signaling networks in higher plants.     

Membrane proteins involved in pollen-pistil interactions.

Self-incompatibility (SI) is a widespread mechanism in angiosperms which prevents self-fertilization. This mechanism relies on cell-cell interactions between pollen and pistil. Among the different SI systems that have been reported, two have been particularly investigated: the gametophytic system of Solanaceae and the sporophytic system of Brassicaceae. In these two families, although the molecular bases of SI response are different, secreted and/or membrane-anchored proteins are required for self-pollen rejection. Interestingly, these proteins exhibit two functions: recognition and a catalytic activity. In this review article, we present recent advances which permit a better understanding of how these proteins control the male/female recognition event associated with the SI response.     

Petunia Germinating Pollen S/D3 Interacts with S-RNases in Petunia hybrida Vilm.

Self-Incompatibility （SI） Is a genetic mechanism of self/non-self pollen recognition to prevent self-fertilization In many flowering plants and, In most cases, this is controlled by a multl-allellc S-locus. S-RNase and Slocus F box （SLF） proteins have been shown to be the female and male determinants of gametophytlc selfIncompatibility （GSI）, respectively, In the Solanaceae, Scrophulariaceae and Rosaceae. Nevertheless, It is thought that additional factors are required for the SI response. Herein, we constructed a mature anther cDNA library from a self-Incompatible Petunia hybrida Vllm. line of the S3S3 haplotype. Using AhS2-RNase from Antirrhinum hispanicum as a bait for yeast two-hybrid screening, we found that petunia germinating pollen （PGP） S/D3 was capable of Interacting physically with the bait. However, the Interaction lacked haplotype specificity. The PGPS/D3 gene Is a single copy gene that Is expressed In tissues such as the style, ovary, pollen, and leaf. The PGPS/D3：：GFP （green fluorescence protein） construct was detected In both the membrane and cytoplasm. The Implications of these findings In the operation of S-RNase-based SI are discussed.     

显花植物自体和异体花粉识别的分子机理研究(英文)

显花植物的受精涉及许多识别过程;其中第一个是雌性生殖组织心皮对花粉的识别。自交不亲和性（Ｓｅｌｆ－ｉｎｃｏｍｐａｔｉｂｉｌｉｔｙ,ＳＩ）是一种广泛分布于显花植物的种内生殖障碍。在多数自交不亲和的植物中,ＳＩ的遗传控制比较简单,受控于一个由复等位基因构成的单一位点,称为Ｓ位点。在以茄科、玄参科和蔷薇科为代表的配子体自交不亲和植物中,Ｓ位点编码一类核酸酶,即Ｓ核酸酶（Ｆｉｇ．１）,控制ＳＩ在花柱中的表达,但是与花粉自交不亲和性的表达无关。后者可能由与Ｓ核酸酶不同的基因控制,这种基因常被称为花粉Ｓ基因。它是目前了解显花植物花粉识别生化和分子机理的关键。近来;通过对影响花粉ＳＩ表达突变体的分子遗传分析提出了一个花粉Ｓ基因产物如何与Ｓ核酸酶相互作用完成自体和异体花粉识别过程的模型（Ｆｉｇ．２）。另外,描述了两个在金鱼草中克隆花粉Ｓ基因的方法,即Ｓ位点选择性的转座子标记和图位克隆。     

四川短尾鼩尿液气味在社会等级识别中的作用

本文在中立竞技场中通过两两互作确定四川短尾鼩(Anourosorex squamipes)同性个体间的社会等级,并在此基础上利用其尿液,研究不同社会等级个体的自我/非自我识别能力及模式、尿液气味的行为响应机制,以及社会等级识别能力。结果表明：(1)四川短尾鼩优势个体表现攻击行为较多,从属个体防御行为较多,优势个体的标记行为显著高于从属个体。攻击行为表现为同等级雄性高于同等级雌性,且雌性间的攻击强度低于雄性。(2)从属个体和优势个体分别对自身尿液气味和非自身尿液气味存在明显偏好差异。不同性别、等级个体自我识别模式差异不明显,不同社会等级个体对于自身识别模式和非自身尿液的行为反应模式均不同。不同社会等级个体具有自我识别能力且能力不同。(3)四川短尾鼩能够识别不同社会等级个体的尿液气味,雌性对雄性尿液更感兴趣,雄性对优势雄性尿液选择回避。雄性对其他个体的访问时间与嗅舔频次均显著高于雌性,雌雄个体在识别不同社会等级的尿液气味时存在性二型。     

Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond

Many hermaphrodite flowering plants avoid self-fertilization through genetic systems of self-incompatibility (SI). SI allows a plant to recognize and to reject self or self-related pollen, thereby preserving its ovules for outcrossing. Genes situated at the S-locus encode the ‘male’ (pollen) and ‘female’ (pistil) recognition determinants of SI. In sporophytic SI (SSI) the male determinant is expressed in the diploid anther, therefore haploid pollen grains behave with a diploid S phenotype. In Brassica, the male and the female determinants of SSI have been identified as a peptide ligand and its cognate receptor, respectively, and recent studies have identified downstream signalling molecules involved in pollen rejection. It now needs to be established whether the Brassica mechanism is universal in species with SSI, or unique to the Brassicaceae.     

At the Root of the Wood Wide Web: Self Recognition and Non-Self Incompatibility in Mycorrhizal Networks

Arbuscular mycorrhizal (AM) fungi are mutualistic symbionts living in the roots of 80% of land plant species, and developing extensive, below-ground extraradical hyphae fundamental for the uptake of soil nutrients and their transfer to host plants. Since AM fungi have a wide host range, they are able to colonize and interconnect contiguous plants by means of hyphae extending from one root system to another. Such hyphae may fuse due to the widespread occurrence of anastomoses, whose formation depends on a highly regulated mechanism of self recognition. Here, we examine evidences of self recognition and non-self incompatibility in hyphal networks formed by AM fungi and discuss recent results showing that the root systems of plants belonging to different species, genera and families may be connected by means of anastomosis formation between extraradical mycorrhizal networks, which can create indefinitely large numbers of belowground fungal linkages within plant communities.Key Words: arbuscular mycorrhizal symbiosis, extraradical mycelium, anastomosis, plant interconnectedness, self recognition, non-self incompatibility, mycorrhizal networks     

A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species

Many flowering plants have evolved self-incompatibility (SI) systems to prevent inbreeding. In the Brassicaceae, SI is genetically controlled by a single polymorphic locus, termed the S-locus. Pollen rejection occurs when stigma and pollen share the same S-haplotype. Recognition of S-haplotype specificity has recently been shown to involve at least two S-locus genes, S-receptor kinase (SRK) and S-locus protein 11 or S-locus Cys-rich (SP11/SCR). SRK encodes a polymorphic membrane-spanning protein kinase, which is the sole female determinant of the S-haplotype specificity. SP11/SCR encodes a highly polymorphic Cys-rich small basic protein specifically expressed in the anther tapetum and in pollen. In cauliflower (B. oleracea), the gain-of-function approach has demonstrated that an allele of SP11/SCR encodes the male determinant of S-specificity. Here we examined the function of two alleles of SP11/SCR of B. rapa by the same approach and further established that SP11/SCR is the sole male determinant of SI in the genus Brassica sp. Our results also suggested that the 522-bp 5'-upstream region of the S9-SP11 gene used to drive the transgene contained all the regulatory elements required for the unique sporophytic/gametophytic expression observed for the native SP11 gene. Promoter deletion analyses suggested that the highly conserved 192-bp upstream region was sufficient for driving this unique expression. Furthermore, immunohistochemical analyses revealed that the protein product of the SP11 transgene was present in the tapetum and pollen, and that in pollen of late developmental stages, the SP11 protein was mainly localized in the pollen coat, a finding consistent with its expected biological role.     

Molecular evolution of the s locus controlling mating in the brassicaceae

Flowering plants possess self-incompatibility (SI) mechanisms that promote outbreeding and thereby increase their genetic diversity. In the self-incompatible Brassicaceae, recognition and rejection of self-pollen is based on a receptor-ligand interaction between male and female SI determinants. A transmembrane receptor kinase (S locus Receptor Kinase, SRK) determines the SI specificity in stigmatic cells, whereas a pollen coat-localized ligand (S locus Cysteine-Rich, SCR) determines the SI specificity in pollen. During recent years, major advances have been made in the understanding of the molecular basis of self-pollen recognition by stigmatic cells. In this review, we will focus on evolutionary aspects of the SI system in Brassicaceae. We will describe how the study of the molecular aspect of SI, not only in the historical Brassica model but also in Arabidopsis species, has contributed to highlight certain aspects of evolution of SI in the Brassicaceae.     

Molecular recognition between glyconectins as an adhesion self-assembly pathway to multicellularity

The appearance of multicellular forms of life has been tightly coupled to the ability of an organism to retain its own anatomical integrity and to distinguish self from non-self. Large glycoconjugates, which make up the outermost cell surface layer of all Metazoans, are the primary candidates for the primordial adhesion and recognition functions in biological self-assembly systems. Atomic force microscopy experiments demonstrated that the binding strength between a single pair of Porifera cell surface glyconectin 1 glycoconjugates from Microciona prolifera can hold the weight of 1600 cells, proving their adhesion functions. Here, measurement of molecular self-recognition of glyconectins (GNs) purified from three Porifera species was used as an experimental model for primordial xenogeneic self/non-self discrimination. Physicochemical and biochemical characterization of the three glyconectins, their glycans, and peptides using gel electrophoresis, ultracentrifugation, NMR, mass spectrometry, glycosaminoglycan-degrading enzyme treatment, amino acid and carbohydrate analyses, and peptide mapping showed that GNs define a new family of proteoglycan-like molecules exhibiting species-specific structures with complex and repetitive acidic carbohydrate motives different from the classical proteoglycans and mucins. In functional self-assembly color-coded bead, cell, and blotting assays, glyconectins displayed species-specific recognition and adhesion. Affinity-purified monospecific polyclonal antibodies prepared against GN1, -2, and -3 glycans selectively inhibited cell adhesion of the respective sponge species. These results together with species-specific coaggregation of GN carbohydrate-coated beads with cells showed that GN glycans are functional in cell recognition and adhesion. The specificity of carbohydrate-mediated homophilic GN interactions in Porifera approaches the binding selectivity of the evolutionarily advanced immunoglobulin superfamily. Xenoselectivity of primordial glyconectin to glyconectin recognition may be a new paradigm in the self-assembly and non-self discrimination pathway of cellular adhesion leading to multicellularity.     

被子植物性系统及其可塑性

繁殖是生物适合度的最终表现,有性繁殖相关性状的多态性极大地促进了物种分化和生物多样性的维持,并影响着植物对环境变化的响应。在种群水平上,被子植物的花有雌花、雄花和两性花三种性表型,三种性表型在种群中的分布和频率即定义了种群的性系统。被子植物的性系统包含植物影响性分配和交配的相关特性,决定着雌配子、雄配子在种群中的频率、交配机会及交配方式,是有性繁殖的关键性状,在被子植物中表现出丰富的多态性,在种群水平上分为性单态和性多态两大类。性单态为被子植物的古老性状,而性多态在100多个被子植物科中独立进化产生。被子植物性系统多态性及其变化机理一直是进化生物学与生态学的热点问题之一。该文以种群水平的性多态为对象,总结了被子植物性系统的类型、表达的遗传基础、分布频率,以及遗传因子、非生物环境和交配环境对性系统表达和性分配的影响。     

基于S- 核酸酶的自交不亲和性的分子机制

自交不亲和性是一种广泛存在于显花植物中的种内生殖障碍, 可以抑制近亲繁殖而促进异交。其中, 以茄科、玄参科和蔷薇科为代表的配子体自交不亲和性是最常见的类型。这类自交不亲和性是由单一的多态性S-位点所控制。目前的研究发现这一位点至少包含两个自交不亲和反应特异性决定因子: 花柱中的S-核酸酶和花粉中的SLF(S-Locus F-box)蛋白。该文将主要介绍并讨论基于S-核酸酶的自交不亲和性分子机制的研究进展。     

Effect of physiological integration in self/non-self genotype recognition on the clonal invader Carpobrotus edulis

Aims Biological invasions represent one of the most important threats to the conservation of biodiversity; however, the mechanisms underlying successful invaders remain unsolved. Many of the most aggressive invaders show clonal growth, and capacity for clonal integration has been pointed out recently as an important trait explaining the success of invasive plants. We aim to determine the role of physiological integration in the capacity for self/non-self genotype recognition in the clonal invader Carpobrotus edulis and the implications of this capacity for the expansion of this aggressive invader.Methods We used connected and severed ramets of identical or different genotype and we determined the capacity for self/non-self recognition by comparing changes in biomass partitioning to avoid competition for resources between pairs of ramets.Important findings Physiological integration allowed self/non-self genotype recognition in the invader C. edulis. Results showed a significant effect of physiological integration on the biomass allocated to roots by genetically identical ramets: older ramets specialize in acquisition of soil-based resources and younger ramets specialize in lateral expansion. This specialization could be considered a form of division of labour, which reduce intra-genotype competition. This is the first evidence that division of labour could be interpreted as a form of self/non-self recognition between genetically identical ramets. Capacity for self/non-self discrimination could contribute to increase the colonization capacity of the aggressive invader C. edulis. This is the first study showing an association between self/non-self recognition and invasiveness in a clonal plant.     

Self- and cross-fertilization in the solitary ascidian Ciona savignyi

Solitary ascidians are hermaphrodites that release sperm and eggs simultaneously. However, many species are self-sterile, owing to a self/non-self recognition system operating at the outer surface of the chorion during sperm-egg interaction. In Ciona intestinalis, self-incompatibility is thought to have a genetic basis. Here, we report a survey of the self-fertilization potential of a Santa Barbara, California, population of Ciona savignyi, a close relative of C. intestinalis. We found that, in contrast to reports on C. intestinalis, C. savignyi is highly self-fertile. However, using two nonlethal recessive mutant strains, aimless (aim) and immaculate (imc), and a stable transgenic strain that expresses green fluorescent protein (GFP) in the notochord to follow offspring genotype, we demonstrate that non-self sperm outcompete self-sperm in fertilization competition assays. When the chorion was removed, both self- and non-self sperm performed equally well in the competition assay. Thus the non-self/self gamete recognition in C. savignyi is not absolute but relative, and is mediated by one or more components in the chorion. We discuss the significance of this finding in the context of natural populations in the wild, where individuals of C. savignyi are typically found growing in large groups that spawn in unison and where self-fertilization would be expected to be very rare.     

Rapid evolution of reproductive proteins in abalone and Drosophila

Observations from different taxa, including plants, protozoa, insects and mammals, indicate that proteins involved in reproduction evolve rapidly. Several models of adaptive evolution have been proposed to explain this phenomenon, such as sexual conflict, sexual selection, self versus non-self recognition and pathogen resistance. Here we discuss the potential role of sexual conflict in the rapid evolution of reproductive genes in two different animal systems, abalone (Haliotis) and Drosophila. In abalone, we reveal how specific interacting sperm-egg proteins were identified and discuss this identification in the light of models for rapid protein evolution and speciation. For Drosophila, we describe the genomic approaches taken to identify male accessory gland proteins and female reproductive tract proteins. Patterns of protein evolution from both abalone and Drosophila support the predicted patterns of rapid protein evolution driven by sexual conflict. We stress however that other selective pressures may contribute to the rapid evolution that is observed. We conclude that the key to distinguishing between sexual conflict and other mechanisms of protein evolution will be an integration of genetic, experimental and theoretical data.     

基于S-核酸酶的自交不亲和性的分子机制

自交不亲和性是一种广泛存在于显花植物中的种内生殖障碍,可以抑制近亲繁殖而促进异交。其中,以茄科、玄参科和蔷薇科为代表的配子体自交不亲和性是最常见的类型。这类自交不亲和性是由单一的多态性S-位点所控制。目前的研究发现这一位点至少包含两个自交不亲和反应特异性决定因子：花柱中的S-核酸酶和花粉中的SLF（S-Locus F-box）蛋白。该文将主要介绍并讨论基于S-核酸酶的自交不亲和性分子机制的研究进展。