Identification of the pollen self-incompatibility determinant in Papaver rhoeas

Wheeler, M. J.; Graaf, Barend H. J. de; Hadjiosif, Natalie; Perry, Ruth M.; Poulter, Natalie S.; Osman, Kim; Vatovec, Sabina; Harper, Andrea L.; Franklin, F. Christopher H.; Franklin‐Tong, Vernonica E.

doi:10.1038/nature08027

Cited by 195 publications

(160 citation statements)

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“…17 In Papaver rhoeas L. (the field poppy), S-determinants are novel, highly polymorphic proteins, PrsS and PrpS. 18,19 PrsS triggers a Ca 2 þ -dependent signalling Self-incompatibility response Self-incompatibility response in incompatible pollen (Papaver rhoeas) Depolymerisation Depolymerisation followed by polymerisation and aggregation into highly stable punctate foci [27][28][29][30][31] Self-incompatibility response in incompatible pollen (Pyrus pyrifolia) A. thaliana leaves/Verticillium dahliae toxins network leading to PCD in incompatible pollen. [20][21][22] There is evidence that ROS, NO 23 and an SI-activated mitogenactivated protein kinase , p56 24 signal to PCD.…”

Section: F-actin and Microtubules Reorganise During Developmental Pcdmentioning

confidence: 99%

Organisation and regulation of the cytoskeleton in plant programmed cell death

2011

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Programmed cell death (PCD) involves precise integration of cellular responses to extracellular and intracellular signals during both stress and development. In recent years much progress in our understanding of the components involved in PCD in plants has been made. Signalling to PCD results in major reorganisation of cellular components. The plant cytoskeleton is known to play a major role in cellular organisation, and reorganization and alterations in its dynamics is a well known consequence of signalling. There are considerable data that the plant cytoskeleton is reorganised in response to PCD, with remodelling of both microtubules and microfilaments taking place. In the majority of cases, the microtubule network depolymerises, whereas remodelling of microfilaments can follow two scenarios, either being depolymerised and then forming stable foci, or forming distinct bundles and then depolymerising. Evidence is accumulating that demonstrate that these cytoskeletal alterations are not just a consequence of signals mediating PCD, but that they also may have an active role in the initiation and regulation of PCD. Here we review key data from higher plant model systems on the roles of the actin filaments and microtubules during PCD and discuss proteins potentially implicated in regulating these alterations.

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Section: F-actin and Microtubules Reorganise During Developmental Pcdmentioning

confidence: 99%

Organisation and regulation of the cytoskeleton in plant programmed cell death

2011

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“…However, hydropathy plot analysis indicated that these proteins may share three to four membrane-spanning domains, and may localize to the plasma membrane of papilla cells, where the interaction between pollen and stigma cells occurs. The structural features of SE proteins are similar to the predicted structure of PrpS proteins, the female determinant of SI of Papaver (Wheeler et al 2009 ), and the fl ower protein of Drosophila (Yao et al 2009 ;Brose and Neher 2009 ), which may act as a Ca 2+ channel in synaptic endocytosis (Fig. 25.11 ).…”

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

confidence: 63%

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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“…PrpS has been shown to be expressed at the plasma membrane, and the predicted extracellular loop of PrpS interacts with PrsS. Use of PrpS antisense oligonucleotides in the pollen in vitro SI bioassay allowed demonstration that PrpS is involved in S -specifi c inhibition of incompatible pollen, providing evidence that it has the biological function expected (Wheeler et al 2009 ).…”

Section: The Pollen S -Locus Determinantsmentioning

confidence: 99%

“…PrpS encodes a novel, small highly hydrophobic protein with a predicted M r ~20 kDa. Examination of the PrpS sequences for nonsynonymous to synonymous ( Ka / Ks ) substitutions revealed no signifi cant difference between substitution rates in PrpS and PrsS genes (Wheeler et al 2009 ). This observation suggests that the pollen and pistil S alleles coevolved, and are likely to be equally ancient, which is an expected characteristic of S -determinants.…”

Section: The Pollen S -Locus Determinantsmentioning

confidence: 99%

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Papaver rhoeas S-Determinants and the Signaling Networks They Trigger

Franklin‐Tong

2014

Sexual Reproduction in Animals and Plants

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Higher plants use specifi c interactions between pollen and pistil to achieve pollination. Self-incompatibility (SI) is an important mechanism used by many species to prevent inbreeding. It is controlled by a multi-allelic S locus. "Self" (incompatible) pollen is discriminated from "non-self" (compatible) pollen by interaction of pollen and pistil S locus components and is subsequently inhibited. Our studies of the SI system in Papaver rhoeas have revealed that the pistil S locus protein, PrsS, is a small novel secreted protein that interacts with the pollen S locus protein, PrpS, which is a small novel transmembrane protein. This interaction of PrsS with incompatible pollen induces a SI response, involving a Ca 2+ -dependent signaling network, resulting in pollen inhibition and programmed cell death; this provides a neat way to destroy "self"-pollen. Several SI-induced events have been identifi ed, including Ca 2+ and K + infl ux, increases in cytosolic free Ca 2+ , activation of a MAP kinase, alterations to the cytoskeleton, and phosphorylation of a soluble inorganic pyrophosphatase. Here we present an overview of our knowledge of the novel cell-cell recognition S -determinants and the signals, targets, and mechanisms triggered by an incompatible interaction. We hope this review is of interest to those involved in the origins and evolution of cell-cell recognition systems involved in discrimination between "self" and "non-self," which include histocompatibility systems in primitive chordates and vertebrates as well as plant self-incompatibility.

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Identification of the pollen self-incompatibility determinant in Papaver rhoeas

Cited by 195 publications

References 37 publications

Organisation and regulation of the cytoskeleton in plant programmed cell death

Organisation and regulation of the cytoskeleton in plant programmed cell death

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

Papaver rhoeas S-Determinants and the Signaling Networks They Trigger

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