The different mechanisms of sporophytic self-incompatibility

Flowering plants have evolved a multitude of mechanisms to avoid self-fertilization and promote outbreeding. Self-incompatibility (SI) is by far the most common of these, and is found in ca. 60% of flowering plants. SI is a genetically controlled pollen-pistil recognition system that provides a barrier to fertilization by self and self-related pollen in hermaphrodite (usually co-sexual) flowering plants. Two genetically distinct forms of SI can be recognized: gametophytic SI (GSI) and sporophytic SI (SSI), distinguished by how the incompatibility phenotype of the pollen is determined. GSI appears to be the most common mode of SI and can operate through at least three different mechanisms, two of which have been characterized extensively at a molecular level in the Solanaceae and Papaveraceae. Because molecular studies of SSI have been largely confined to species from the Brassicaceae, predominantly Brassica species, it is not yet known whether SSI, like GSI, can operate through different molecular mechanisms. Molecular studies of SSI are now being carried out on Ipomoea trifida (Convolvulaceae) and Senecio squalidus (Asteraceae) and are providing important preliminary data suggesting that SSI in these two families does not share the same molecular mechanism as that of the Brassicaceae. Here, what is currently known about the molecular regulation of SSI in the Brassicaceae is briefly reviewed, and the emerging data on SSI in I. trifida, and more especially in S. squalidus, are discussed.     

Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition

Self-incompatibility (SI) prevents the production of “self” seed and inbreeding by providing a recognition and rejection system for “self,” or genetically identical, pollen. Studies of gametophytic SI (GSI) species at a molecular level have identified two completely different S-genes and SI mechanisms. One GSI mechanism, which is found in the Solanaceae, Rosaceae and Scrophulariaceae, has S-RNase as the pistil S-component and an F-box protein as the pollen S-component. However, non-S-locus factors are also required. In an incompatible situation, the S-RNases degrade pollen RNA, thereby preventing pollen tube growth. Here, in the light of recent evidence, we examine alternative models for how compatible pollen escapes this cytotoxic activity. The other GSI mechanism, so far found only in the Papaveraceae, has a small secreted peptide, the S-protein, as its pistil S-component. The pollen S-component remains elusive, but it is thought to be a transmembrane receptor, as interaction of the S-protein with incompatible pollen triggers a signaling network, resulting in rapid actin depolymerization and pollen tube inhibition and programmed cell death (PCD). Here, we present an overview of what is currently known about the mechanisms involved in regulating pollen tube inhibition in these two GSI systems.     

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.     

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。     

Gametophytic self-incompatibility: contrasting mechanisms for Nicotiana and Papaver

Since Darwin first noted that not all plants produce self-seed, several mechanisms that regulate the acceptance or rejection of pollen during fertilization have been recognized, of which self-incompatibility (SI) is the most widespread. Over the past few years much progress has been made in understanding the molecular and cellular processes involved in SI. Here we review recent studies of the SI systems of Nicotiana alata and Papaver rhoeas. The SI systems are both determined by a single, multi-allelic gametophytically controlled S-gene, but involve quite different mechanisms.     

Expression and trans-specific polymorphism of self-incompatibility RNases in coffea (Rubiaceae)

Self-incompatibility (SI) is widespread in the angiosperms, but identifying the biochemical components of SI mechanisms has proven to be difficult in most lineages. Coffea (coffee; Rubiaceae) is a genus of old-world tropical understory trees in which the vast majority of diploid species utilize a mechanism of gametophytic self-incompatibility (GSI). The S-RNase GSI system was one of the first SI mechanisms to be biochemically characterized, and likely represents the ancestral Eudicot condition as evidenced by its functional characterization in both asterid (Solanaceae, Plantaginaceae) and rosid (Rosaceae) lineages. The S-RNase GSI mechanism employs the activity of class III RNase T2 proteins to terminate the growth of "self" pollen tubes. Here, we investigate the mechanism of Coffea GSI and specifically examine the potential for homology to S-RNase GSI by sequencing class III RNase T2 genes in populations of 14 African and Madagascan Coffea species and the closely related self-compatible species Psilanthus ebracteolatus. Phylogenetic analyses of these sequences aligned to a diverse sample of plant RNase T2 genes show that the Coffea genome contains at least three class III RNase T2 genes. Patterns of tissue-specific gene expression identify one of these RNase T2 genes as the putative Coffea S-RNase gene. We show that populations of SI Coffea are remarkably polymorphic for putative S-RNase alleles, and exhibit a persistent pattern of trans-specific polymorphism characteristic of all S-RNase genes previously isolated from GSI Eudicot lineages. We thus conclude that Coffea GSI is most likely homologous to the classic Eudicot S-RNase system, which was retained since the divergence of the Rubiaceae lineage from an ancient SI Eudicot ancestor, nearly 90 million years ago.     

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。     

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。     

The different mechanisms of gametophytic self-incompatibility

Self-incompatibility (SI) involves the recognition and rejection of self or genetically identical pollen. Gametophytic SI is probably the most widespread of the SI systems and, so far, two completely different SI mechanisms, which appear to have evolved separately, have been identified. One mechanism is the RNase system, which is found in the Solanaceae, Rosaceae and Scrophulariaceae. The other is a complex system, so far found only in the Papaveraceae, which involves the triggering of signal transduction cascade(s) that result in rapid pollen tube inhibition and cell death. Here, we present an overview of what is currently known about the mechanisms involved in controlling pollen tube inhibition in these two systems.     

Selection of sporophytic and gametophytic self‐incompatibility in the absence of a superlocus

Self‐incompatibility (SI) is a complex trait that enforces outcrossing in plant populations. SI generally involves tight linkage of genes coding for the proteins that underlie self‐pollen detection and pollen identity specification. Here, we develop two‐locus genetic models to address the question of whether sporophytic SI (SSI) and gametophytic SI (GSI) can invade populations of self‐compatible plants when there is no linkage or weak linkage of the underlying pollen detection and identity genes (i.e., no S‐locus supergene). The models assume that SI evolves as a result of exaptation of genes formerly involved in functions other than SI. Model analysis reveals that SSI and GSI can invade populations even when the underlying genes are loosely linked, provided that inbreeding depression and selfing rate are sufficiently high. Reducing recombination between these genes makes conditions for invasion more lenient. These results can help account for multiple, independent evolution of SI systems as seems to have occurred in the angiosperms.     

How far are we from unravelling self-incompatibility in grasses?

The genetic and physiological mechanisms involved in limiting self-fertilization in angiosperms, referred to as self-incompatibility (SI), have significant effects on population structure and have potential diversification and evolutionary consequences. Up to now, details of the underlying genetic control and physiological basis of SI have been elucidated in two different gametophytic SI (GSI) systems, the S-RNase SI and the Papaver SI systems, and the sporophytic SI (SSI) system (Brassica). In the grass family (Poaceae), which contains all the cereal and major forage crops, SI has been known for half a century to be controlled gametophytically by two multiallelic and independent loci, S and Z. But still none of the gene products for S and Z is known and only limited information on related biochemical responses is available. Here we compare current knowledge of grass SI with that of other well-characterized SI systems and speculate about the relationship between SSI and grass SI. Additionally, we discuss comparative mapping as a tool for the further investigation of grass SI.     

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.     

Progress towards elucidating the mechanisms of self-incompatibility in the grasses: further insights from studies in Lolium

BACKGROUND AND SCOPE: Self-incompatibility (SI) in flowering plants ensures the maintenance of genetic diversity by ensuring outbreeding. Different genetic and mechanistic systems of SI among flowering plants suggest either multiple origins of SI or considerable evolutionary diversification. In the grasses, SI is based on two loci, S and Z, which are both polyallelic: an incompatible reaction occurs only if both S and Z alleles are matched in individual pollen with alleles of the pistil on which they alight. Such incompatibility is referred to as gametophytic SI (GSI). The mechanics of grass GSI is poorly understood relative to the well-characterized S-RNase-based single-locus GSI systems (Solanaceae, Rosaceae, Plantaginaceae), or the Papaver recognition system that triggers a calcium-dependent signalling network culminating in programmed cell death. There is every reason to suggest that the grass SI system represents yet another mechanism of SI. S and Z loci have been mapped using isozymes to linkage groups C1 and C2 of the Triticeae consensus maps in Secale, Phalaris and Lolium. Recently, in Lolium perenne, in order to finely map and identify S and Z, more closely spaced markers have been developed based on cDNA and repeat DNA sequences, in part from genomic regions syntenic between the grasses. Several genes tightly linked to the S and Z loci were identified, but so far no convincing candidate has emerged. RESEARCH AND PROGRESS: From subtracted Lolium immature stigma cDNA libraries derived from S and Z genotyped individuals enriched for SI potential component genes, kinase enzyme domains, a calmodulin-dependent kinase and a peptide with several calcium (Ca(2+)) binding domains were identified. Preliminary findings suggest that Ca(2+) signalling and phosphorylation may be involved in Lolium GSI. This is supported by the inhibition of Lolium SI by Ca(2+) channel blockers lanthanum (La(3+)) and verapamil, and by findings of increased phosphorylation activity during an SI response.     

Do s genes or deleterious recessives control late-acting self-incompatibility in Handroanthus heptaphyllus (Bignoniaceae)? A diallel study with four full-sib progeny arrays

Background and AimsGenetically controlled self-incompatibility (SI) mechanisms constrain selfing and thus have contributed to the evolutionary diversity of flowering plants. In homomorphic gametophytic SI (GSI) and homomorphic sporophytic SI (SSI), genetic control is usually by the single multi-allelic locus S. Both GSI and SSI prevent self pollen tubes reaching the ovary and so are pre-zygotic in action. In contrast, in taxa with late-acting self-incompatibility (LSI), rejection is often post-zygotic, since self pollen tubes grow to the ovary, where fertilization may occur prior to floral abscission. Alternatively, lack of self fruit set could be due to early-acting inbreeding depression (EID). The aim of our study was to investigate mechanisms underlying the lack of selfed fruit set in Handroanthus heptaphyllus in order to assess the likelihood of LSI versus EID.MethodsWe employed four full-sib diallels to study the genetic control of LSI in H. heptaphyllus using a precociously flowering variant. We also used fluorescence microscopy to study the incidence of ovule penetration by pollen tubes in pistils that abscised following pollination or initiated fruits.Key ResultsAll diallels showed reciprocally cross-incompatible full sibs (RCIs), reciprocally cross-compatible full sibs (RCCs) and non-reciprocally compatible full sibs (NRCs) in almost equal proportions. There was no significant difference between the incidences of ovule penetrations in abscised pistils following self- and cross-incompatible pollinations, but those in successful cross-pollinations were around 2-fold greater.ConclusionsA genetic model postulating a single S locus with four S alleles, one of which, in the maternal parent, is dominant to the other three, will produce RCI, RCC and NRC full sib situations each at 33 %, consistent with our diallel results. We favour this simple genetic control over an EID explanation since none of our pollinations, successful or unsuccessful, resulted in partial embryo development, as would be expected under a whole-genome EID effect.     

Molecular Determinants and Mechanisms of Gametophytic Self-Incompatibility in Fruit Trees of Rosaceae

Self-incompatibility is an important genetic mechanism that prevents inbreeding and promotes genetic polymorphism and heterosis in flowering plants. Many fruit species in the Rosaceae, including apple, pear, plum, apricot, sweet cherry, Japanese apricot, and almond, exhibit typical gametophytic self-incompatibility (GSI) controlled by an apparently single multi-allelic locus. This locus encodes at least two components from both the pollen and the pistil, and controls recognition of self- and non-self pollen. Recently, the GSI system has been investigated at the molecular and cellular levels in Rosaceae, and findings have provided some important insights as to how these two genes interact within pollen tubes that lead to specific inhibition of germination and/or growth of self-pollen tubes. In this review, molecular features of S-determinants of both pistil and pollen, identification of S-alleles, mechanisms of self-incompatibility break-down, and evolution of S-alleles are presented. Moreover, hypothetical signal transduction models in a self-incompatible system in Rosaceae are proposed based on recent findings that indicate that several signal factors are involved in GSI responses.     

Disentangling the components of pollen limitation in a widespread herb with gametophytic self-incompatibility

Premise

Seed production is frequently limited by the receipt of insufficient or low-quality pollen, collectively termed “pollen limitation” (PL). In taxa with gametophytic self-incompatibility (GSI), incompatible pollen can germinate on stigmas but pollen tubes are arrested in styles. This allows for estimates of pollen performance before, during, and after self-recognition, as well as insight into the factors underlying pollen quality limitation in GSI taxa.

Methods

We scored pollen performance following self and outcross pollinations in Argentina anserina to identify the location of self-recognition and establish the relationship between pollen tubes and seed production. We then estimated quantity and quality components of PL from >3300 field-collected styles. We combined our results with other studies to test the prediction that low pollen quality, but not quantity, drives higher PL in self-incompatible (SI) taxa than in self-compatible taxa (SC).

Results

Self and outcross pollen germinated readily on stigmas, but 96% of germinated self-pollen was arrested during early tube elongation. Reproduction in the field was more limited by pollen quality than by quantity, and pollen failure near the location of self-recognition was a stronger barrier to fertilization than pollen germination. Across 26 taxa, SI species experienced stronger pollen quality, but not quantity, limitation than SC species.

Conclusions

Evaluating pollen performance at multiple points within pistils can elucidate potential causes of pollen quality limitation. The receipt of incompatible pollen inhibits fertilization success more than insufficient pollen receipt or poor pollen germination in A. anserina. Likewise, pollen quality limitation drives high overall PL in other SI taxa.     

The Diversity of Self-Incompatibility Systems in Flowering Plants

Abstract: Flowering plants are the most successful group of land plants and dominate the earth's vegetation with around 300 000 species. This success is, in part, the consequence of a set of unique reproductive innovations that evolved with the flower. Most notable of these innovations were the closed carpel and double fertilization. Closed carpels permitted the evolution of effective mechanisms for pollen selection and discrimination, while double fertilization leading to endosperm formation allowed for more efficient utilization of resources because reserves are only allocated to the seed after fertilization. This review will focus on the most important and best understood mechanism of pollen discrimination, self-incompatibility (SI), a genetically determined pollen recognition system that prevents self-fertilization and fertilization by other individuals with the same incompatibility phenotype. In recent years much progress has been made towards elucidating the molecular mechanisms of SI operating in three distinct SI systems found in the Brassicaceae, Solanaceae and Papaveraceae, respectively. More recent molecular data obtained from the Poaceae, Convolvulaceae and Asteraceae, however, suggest that other molecular mechanisms of SI exist. A survey of classical genetic studies of SI predicts yet further potential molecular mechanisms of SI. We discuss the evolutionary implications of this apparent diversity in molecular pathways leading to SI and stress the need for more molecular studies of different SI systems.     

Sequence divergence and loss-of-function phenotypes of S locus F-box brothers genes are consistent with non-self recognition by multiple pollen determinants in self-incompatibility of Japanese pear (Pyrus pyrifolia)

The S-RNase-based gametophytic self-incompatibility (SI) of Rosaceae, Solanaceae, and Plantaginaceae is controlled by at least two tightly linked genes located at the complex S locus; the highly polymorphic S-RNase for pistil specificity and the F-box gene (SFB/SLF) for pollen. Self-incompatibility in Prunus (Rosaceae) is considered to represent a 'self recognition by a single factor' system, because loss-of-function of SFB is associated with self-compatibility, and allelic divergence of SFB is high and comparable to that of S-RNase. In contrast, Petunia (Solanaceae) exhibits 'non-self recognition by multiple factors'. However, the distribution of 'self recognition' and 'non-self recognition' SI systems in different taxa is not clear. In addition, in 'non-self recognition' systems, a loss-of-function phenotype of pollen S is unknown. Here we analyze the divergence of SFBB genes, the multiple pollen S candidates, of a rosaceous plant Japanese pear (Pyrus pyrifolia) and show that intrahaplotypic divergence is high and comparable to the allelic diversity of S-RNase while interhaplotypic divergence is very low. Next, we analyzed loss-of-function of the SFBB1 type gene. Genetic analysis showed that pollen with the mutant haplotype S(4sm) lacking SFBB1-S(4) is rejected by pistils with an otherwise compatible S(1) while it is accepted by other non-self pistils. We found that the S(5) haplotype encodes a truncated SFBB1 protein, even though S(5) pollen is accepted normally by pistils with S(1) and other non-self haplotypes. These findings suggest that Japanese pear has a 'non-self recognition by multiple factors' SI system, although it is a species of Rosaceae to which Prunus also belongs.