The S receptor kinase determines self-incompatibility in Brassica stigma

Takasaki, Takeshi; Hatakeyama, Katsunori; Suzuki, Go; Watanabe, Masao; Isogai, Akira; Hinata, Kokichi

doi:10.1038/35002628

Cited by 514 publications

(378 citation statements)

References 28 publications

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“…However, the apparently general use of a polyadenylation signal within the first intron of SRK and SRK-like genes is suggestive of some functional significance for the soluble form of the receptor domain. It is possible that in A. lyrata, as well as in the self-incompatible Brassica plants that lack SLG or express low levels of SLG, the soluble form of SRK fulfills a role similar to that proposed for SLG and functions to enhance the SI response (Dixit et al, 2000;Takasaki et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

“…The function of SLG is not well understood, and its role in SI has been questioned (Cabrillac et al, 1999;Nasrallah, 2000;Nishio and Kusaba, 2000). However, recent studies have indicated that SLG enhances the intensity of the SI response (Takasaki et al, 2000), possibly by contributing to the proper maturation of the SRK receptor and its accumulation to physiologically relevant levels (Dixit et al, 2000).…”

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confidence: 99%

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Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana

Kusaba¹,

Dwyer²,

Hendershot³

et al. 2001

The Plant Cell

131

282

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As a starting point for a phylogenetic study of self-incompatibility (SI) in crucifers and to elucidate the genetic basis of transitions between outcrossing and self-fertilizing mating systems in this family, we investigated the SI system of Arabidopsis lyrata . A. lyrata is an outcrossing close relative of the self-fertile A. thaliana and is thought to have diverged from A. thaliana ‫ف‬ 5 million years ago and from Brassica spp 15 to 20 million years ago. Analysis of two S (sterility) locus haplotypes demonstrates that the A. lyrata S locus contains tightly linked orthologs of the S locus receptor kinase ( SRK ) gene and the S locus cysteine-rich protein ( SCR ) gene, which are the determinants of SI specificity in stigma and pollen, respectively, but lacks an S locus glycoprotein gene. As described previously in Brassica , the S haplotypes of A. lyrata differ by the rearranged order of their genes and by their variable physical sizes. Comparative mapping of the A. lyrata and Brassica S loci indicates that the S locus of crucifers is a dynamic locus that has undergone several duplication events since the Arabidopsis-Brassica split and was translocated as a unit between two distant chromosomal locations during diversification of the two taxa. Furthermore, comparative analysis of the S locus region of A. lyrata and its homeolog in self-fertile A. thaliana identified orthologs of the SRK and SCR genes and demonstrated that self-compatibility in this species is associated with inactivation of SI specificity genes. INTRODUCTIONSelf-incompatibility (SI) is the major outcrossing mechanism in the family Brassicaceae (de Nettancourt, 1977). Species in this family have been grouped into 19 tribes on the basis of morphological criteria (Schultz, 1936), and SI has been described in all tribes analyzed to date. When Bateman (1955) surveyed 182 species distributed in 11 tribes, he found that approximately half of these species included selfincompatible accessions. In a survey of 59 taxa in the subtribe Brassicineae of the tribe Brassiceae (which includes Brassica and Raphanus ), 50 taxa were self-incompatible (Takahata and Hinata, 1980). In all cases analyzed, SI has been shown to be controlled sporophytically by a single S (sterility) locus, with multiple alleles or variants and complex dominance relationships between alleles (Bateman, 1954(Bateman, , 1955Thompson and Taylor, 1966): in self-incompatible plants, pollen will not develop on a stigma that expresses the same S alleles as the pollen parent.Molecular analysis of the Brassica S locus region has shown that this mendelian locus is a gene complex consisting of distinct stigma-expressed and anther-expressed genes that determine SI specificity in stigma and pollen, respectively (reviewed in Nasrallah, 2000). The SRK (for S locus receptor kinase) gene (Stein et al., 1991) encodes a plasma membrane-spanning receptor serine/threonine kinase specific to the stigma epidermis (Stein et al., 1996) and is the determinant of SI specificity in the stigma (Takasaki et al., 2000). ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana

Kusaba¹,

Dwyer²,

Hendershot³

et al. 2001

The Plant Cell

131

282

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“…In the SSI system of Brassica , SLG and SRK genes are expressed in the mature papilla cells of the stigma (Nasrallah and Nasrallah 1993 ). The expression of SRK is signifi cantly lower than SLG ; however, SRK plays a key role in the self-pollen recognition of Brassica (Takasaki et al 2000 ). The male S -gene in Brassica , SP11 / SCR , is tightly linked to the SRK gene at the S -locus and is expressed in the anther tapetum (the sporophytic tissue) and microspores at a late developmental stage of pollen grains (Schopfer et al 1999 ;Takayama et al 2000 ;Shiba et al 2002 ).…”

Section: Genes Located At or Near The S -Locus Of I Trifi Damentioning

confidence: 99%

“…Because I. trifi da has the same genetic SI system as Brassica species, it might be expected that products of genes homologous to SLG or SRK would be present in the reproductive tissues of I. trifi da. SRK is known as a female S -gene (Stein et al 1991 ;Takasaki et al 2000 ), and SLG is an S -gene-related gene in Brassica (Kandasamy et al 1989 ). Ipomoea secreted glycoprotein genes ( ISG1 , -2 , and -3 ) were isolated from a mature stigma cDNA library, and the sequences of these genes showed structural similarities to Brassica SLGs.…”

Section: Several Approaches To Identifying S -Genes In I Trifi Damentioning

confidence: 99%

Self-Incompatibility System of Ipomoea trifida, a Wild-Type Sweet Potato

Tsuchiya

2014

Sexual Reproduction in Animals and Plants

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Diploid Ipomoea trifi da (Convolvulaceae) is a close relative of the cultivated hexaploid Ipomoea batatas , the cultivated sweet potato. These plants have sporophytic self-incompatibility that is regulated by a single multiallelic locus, designated as the S -locus. Genetic analyses of I. trifi da plants collected from Central America identifi ed about 50 different S -haplotypes with a linear dominance hierarchy having some codominance relationships. A linkage map of DNA markers around the S -locus indicated that the S -locus is delimited to 0.23 cM. Within the S -locus genomic region, a hypervariable genomic region of 35-95 kbp was identifi ed, and we designated this region SDR ( S -locus-specifi c divergent region). Of the several genes located within the SDR, one anther-specifi c gene, AB2 , and three stigma-specifi c genes, SE1 , SE2 , and SEA , are candidate S -genes that may encode male and female S -determinants of self-incompatibility.Keywords Ipomoea trifi da • Self-incompatibility • Sweet potato IntroductionSelf-incompatibility (SI) is a genetic mechanism to prevent self-fertilization (and thus encourage outcrossing) in angiosperms. In self-incompatible plants, when a pollen grain is recognized as the same type as self, some stage of pollen germination, pollen tube elongation, ovule fertilization, or embryo development is halted, and no seeds are produced. SI is classifi ed into several groups: homomorphic SI, heteromorphic SI, cryptic SI (CSI), and late-acting SI. Heteromorphic SI is classifi ed into two groups: distyly is determined by a single locus, which has two alleles, and tristyly is determined by two loci, each with two alleles. Heteromorphic SI is sporophytic, in that both alleles in the male plant determine the SI response in the pollen. CSI exists in a limited number of taxa (for example, there is evidence for CSI in Silene vulgaris in the Caryophyllaceae; Glaettli 2004 ). In this mechanism, the simultaneous presence of cross-and self-pollen on the same stigma results in higher seed set from cross-pollen (Bateman 1956 ). Late-acting SI is also termed ovarian SI. In this mechanism, self-pollen germinates and reaches the ovules, but no fruit is set (Seavey and Bawa 1986 ;Sage et al. 1994 ).Homomorphic SI is classifi ed into sporophytic SI (SSI) and gametophytic SI (GSI) . The SSI system is found in species of several plant families, such as the Brassicaceae, Asteraceae, Malvaceae, Betulaceae, Sterculiaceae, Polemoniaceae, and Convolvulaceae (de Nettancourt 2001 ; Allen and Hiscock 2008 ). In the plants in these families, SI is genetically regulated by a single multi-allelic locus, the S -locus . Within the S -locus, a pair of genes (named S -genes ), one encoding the male-determinant molecules and the other the female-determinant molecules, is localized. These genes are essential for the SI reaction, because these gene products contribute to self/non-self recognition. The sets of S -genes are tightly linked at the S -locus, and the S -locus (also called S -haplotype : Nasrallah and Na...

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“…The female determinant is S -receptor kinase (SRK) (Takasaki et al 2000 ). SRK consists of an SLG-like extracellular domain, a transmembrane domain, and an intracellular serine/threonine kinase domain.…”

Section: Self/non-self Recognition System In the Brassicaceaementioning

confidence: 99%

Self-Incompatibility in the Brassicaceae

Iwano

Itô

Shimosato-Asano

et al. 2014

Sexual Reproduction in Animals and Plants

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Self-incompatibility (SI) in angiosperms prevents inbreeding and promotes outcrossing to generate genetic diversity. SI in the Brassicaceae is controlled by the S -haplotype-specifi c interaction between pollen ligand ( S -locus protein 11, SP11 or SCR) and its stigmatic receptor ( S -receptor kinase, SRK ). SP11/ SCR binding to cognate SRK induces autophosphorylation of SRK, which triggers a signaling cascade leading to the rejection of self-pollen. However, the mechanism of self-pollen rejection downstream of this ligand-receptor interaction is unknown. Here, we generated self-incompatible Arabidopsis thaliana accession C24 for the forward-genetic approach and live-cell imaging of SI in the Brassicaceae. Furthermore, for reverse-genetic analysis, we extended the Arabidopsis Targeting Induced Local Lesions IN Genomes (TILLING) resources by developing a new population of ethyl methanesulfonate (EMS)-induced mutant lines in A. thaliana accession C24. We believe that the reverse-genetic approach is a useful tool for identifying genes that function in the SI signaling pathway of the Brassicaceae.

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The S receptor kinase determines self-incompatibility in Brassica stigma

Cited by 514 publications

References 28 publications

Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana

Self-Incompatibility in the Genus Arabidopsis: Characterization of the S Locus in the Outcrossing A. lyrata and Its Autogamous Relative A. thaliana

Self-Incompatibility System of Ipomoea trifida, a Wild-Type Sweet Potato

Self-Incompatibility in the Brassicaceae

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