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Identification Of The Pollen Self-incompatibility Determinant In Papaver Rhoeas

M. Wheeler, B. H. D. de Graaf, Natalie Hadjiosif, Ruth M. Perry, N. S. Poulter, K. Osman, S. Vatovec, Andrea L. Harper, F. H. Franklin, V. Franklin-Tong
Published 2009 · Biology, Medicine

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Higher plants produce seed through pollination, using specific interactions between pollen and pistil. Self-incompatibility is an important mechanism used in 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. In Papaver rhoeas, the pistil S locus product is a small protein that interacts with incompatible pollen, triggering a Ca2+-dependent signalling network, resulting in pollen inhibition and programmed cell death. Here we have cloned three alleles of a highly polymorphic pollen-expressed gene, PrpS (Papaver rhoeas pollen S), from Papaver and provide evidence that this encodes the pollen S locus determinant. PrpS is a single-copy gene linked to the pistil S gene (currently called S, but referred to hereafter as PrsS for Papaver rhoeas stigma S determinant). Sequence analysis indicates that PrsS and PrpS are equally ancient and probably co-evolved. PrpS encodes a novel ∼20-kDa protein. Consistent with predictions that it is a transmembrane protein, PrpS is associated with the plasma membrane. We show that a predicted extracellular loop segment of PrpS interacts with PrsS and, using PrpS antisense oligonucleotides, we demonstrate that PrpS is involved in S-specific inhibition of incompatible pollen. Identification of PrpS represents a major advance in our understanding of the Papaver self-incompatibility system. As a novel cell–cell recognition determinant it contributes to the available information concerning the origins and evolution of cell–cell recognition systems involved in discrimination between self and non-self, which also include histocompatibility systems in primitive chordates and vertebrates.
This paper references
10.1038/nature05311
Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen
B. J. D. Graaf (2006)
10.1038/232230A0
“Self-recognition” in Colonial Marine Forms and Flowering Plants in relation to the Evolution of Immunity
F. Burnet (1971)
10.1046/J.1365-313X.2000.00811.X
Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas.
N. D. Jordan (2000)
10.1007/978-3-540-68486-2
Self-Incompatibility in Flowering Plants
V. E. Franklin-Tong (2008)
10.1007/BF00020809
Molecular analysis of two functional homologues of the S3 allele of the Papaver rhoeas self-incompatibility gene isolated from different populations
E. Walker (2004)
10.1046/J.1432-1033.2003.03762.X
Mapping the binding domains of the αIIb subunit
N. Biris (2003)
10.1111/J.1432-1033.1988.TB14150.X
Topogenic signals in integral membrane proteins.
G. von Heijne (1988)
Evolution, Diversity, and Mechanisms (ed
Kohn (2008)
puzzled by pollen S
E. Newbigin (2008)
The F-box protein AhSLF-S2 controls the pollen function of S-RNasebased self-incompatibility
H Qiao (2004)
10.1038/nature04150
Isolation and characterization of a protochordate histocompatibility locus
A. D. Tomaso (2005)
Author manuscript; available in PMC
(2009)
10.1038/066234b0
STATISTICAL METHODS IN BIOLOGY
Lingsong Zhang (1902)
Microtubules are a target for self-incompatibility signaling in Papaver pollenPubMed: 18192439] 38 Self-incompatibility in Papaver rhoeas.1. Characterization of the stigmatic component
Ns Poulter (1988)
10.1007/s00425-006-0284-2
Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition
B. McClure (2006)
Signal-mediated depolymerization of actin in pollen during the selfincompatibility response
B. N. Snowman (2002)
Self-incompatibility in Papaver rhoeas
V. E. Franklin-Tong (1988)
10.1073/PNAS.87.24.9732
Polymorphism at the self-incompatibility locus in Solanaceae predates speciation.
T. Ioerger (1990)
10.1046/J.1432-1033.2003.03762.X
Mapping the binding domains of the alpha(IIb) subunit. A study performed on the activated form of the platelet integrin alpha(IIb)beta(3).
N. Biris (2003)
10.1016/S0022-2836(05)80360-2
Basic local alignment search tool.
S. Altschul (1990)
The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based selfincompatibility
H Qiao (2004)
10.1073/PNAS.91.6.2265
Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas L.
H. C. Foote (1994)
10.1002/BIES.950170108
Multi‐allelic self‐incompatibility polymorphisms in plants
D. Charlesworth (1995)
10.1083/jcb.200604011
Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen
S. Thomas (2006)
10.1093/bioinformatics/17.7.646
Evaluation of methods for the prediction of membrane spanning regions
S. Möller (2001)
10.1038/hdy.1978.24
The genetical control of self-incompatibility in Papaver rhoeas
M. J. Lawrence (1978)
DNA polymorphism analyses by the coalescent and other methods
J. Rozas (2003)
10.1111/J.1469-8137.1989.TB02386.X
Characterization of a stigmatic component from Papaver rhoeas L. which exhibits the specific activity of a self‐incompatibility (S–) gene product
V. E. Franklin-Tong (1989)
10.1093/bioinformatics/btg359
DnaSP, DNA polymorphism analyses by the coalescent and other methods
J. Rozas (2003)
Statistical Methods and Scientific Inference (Hafner
R. A. Fisher (1956)
10.1146/ANNUREV.ARPLANT.56.032604.144249
Self-incompatibility in plants.
S. Takayama (2005)
Bradford MM. A dye binding assay for protein Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. The Plant Cell
Ra Fisher (1956)
10.1073/PNAS.88.19.8816
Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea.
J. Stein (1991)
10.1093/AOB/MCP250
Self-incompatibility in flowering plants. Evolution, diversity, and mechanisms
D. Charlesworth (2010)
10.1007/s004970050141
Identification and cloning of related self-incompatibility S-genes in Papaver rhoeas and Papaver nudicaule
S. Kurup (1998)
Self - incompatibility in Papaver rhoeas . 1 . Characterization of the stigmatic component
V. E. Franklin-Tong (1988)
10.1016/0003-2697(76)90527-3
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
10.1105/tpc.12.7.1239
Alterations in the Actin Cytoskeleton of Pollen Tubes Are Induced by the Self-Incompatibility Reaction in Papaver rhoeas
A. Geitmann (2000)
The F-box protein AhSLF-S 2 controls the pollen function of S-RNase-based selfincompatibility . The Plant Cell
H Qiao (2004)
10.1046/J.1365-313X.1993.04010163.X
The self‐incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium
V. E. Franklin-Tong (1993)
Author manuscript; available in PMC
(2009)
10.1105/tpc.002998
Signal-Mediated Depolymerization of Actin in Pollen during the Self-Incompatibility Response Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002998.
B. N. Snowman (2002)
A dye binding assay for protein
M. M. Bradford (1976)
10.1006/JMBI.2000.4315
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
A. Krogh (2001)
10.1038/nature02540
Self-incompatibility triggers programmed cell death in Papaver pollen
S. Thomas (2004)
Microtubules are a target for self-incompatibility signaling in Papaver pollenPubMed: 18192439] 38 Self-incompatibility in Papaver rhoeas.1. Characterization of the stigmatic component
Ns Poulter (1988)
Bradford MM. A dye binding assay for protein Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. The Plant Cell
Ra Fisher (1956)
10.1105/tpc.108.060327
RNase-Based Self-Incompatibility: Puzzled by Pollen S[W]
E. Newbigin (2008)
The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based selfincompatibility
H Qiao (2004)
application to complete genomes
A. Krogh (2001)
10.1038/nature02523
Identification of the pollen determinant of S-RNase-mediated self-incompatibility
Paja Sijacic (2004)
10.1073/pnas.0705826104
Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen
Maurice Bosch (2007)
10.1101/GR.5.2.173
BEAUTY: an enhanced BLAST-based search tool that integrates multiple biological information resources into sequence similarity search results.
K. Worley (1995)
10.1046/J.1365-313X.1996.09040467.X
Identification of a membrane glycoprotein in pollen of Papaver rhoeas which binds stigmatic self‐incompatibility (S‐) proteins
Melanie J. Hearn (1996)
The F-box protein AhSLF-S 2 controls the pollen function of S-RNase-based selfincompatibility . The Plant Cell
H Qiao (2004)
Self-incompatibility in flowering plants : evolution, diversity, and mechanisms
V. E. Franklin-Tong (2008)
10.2307/2342557
Statistical Methods and Scientific Inference
M. Bartlett (1957)
10.1007/978-3-540-68486-2_5
What Genealogies of S-alleles Tell Us
J. Kohn (2008)
10.1105/tpc.104.024919
The F-Box Protein AhSLF-S2 Controls the Pollen Function of S-RNase–Based Self-Incompatibility
Hong Qiao (2004)
10.1104/pp.107.107052
Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen1
N. S. Poulter (2008)
Statistical Methods in Biology (The English Universities Press, 1959)
N.T.J. Bailey (2009)
10.1007/s004970100086
Antisense perturbation of protein function in living pollen tubes
A. Moutinho (2001)
10.1038/35081161
Plant pathogens and integrated defence responses to infection
J. Dangl (2001)
10.1038/295499A0
Protochordate allorecognition is controlled by a MHC-like gene system
V. Scofield (1982)



This paper is referenced by
10.1038/cdd.2011.39
Organisation and regulation of the cytoskeleton in plant programmed cell death
A. Smertenko (2011)
10.3389/fpls.2020.00195
Self-(In)compatibility Systems: Target Traits for Crop-Production, Plant Breeding, and Biotechnology
J. V. Muñoz-Sanz (2020)
10.1266/GGS.85.297
Achievement of genetics in plant reproduction research: the past decade for the coming decade.
Keita Suwabe (2010)
10.3390/ijms20010209
Cytoskeleton, Transglutaminase and Gametophytic Self-Incompatibility in the Malinae (Rosaceae)
S. Del Duca (2019)
10.3390/ijms20092356
Transcriptomic Analysis Reveals a Comprehensive Calcium- and Phytohormone-Dominated Signaling Response in Leymus chinensis Self-Incompatibility
Shuangyan Chen (2019)
10.1093/jxb/err002
Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development.
E. Marshall (2011)
Investigating pollen signalling networks triggered by the self-incompatibility response in Papaver rhoeas
Katie A Wilkins (2013)
10.1111/nph.12180
ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice.
K. Wang (2013)
10.1104/pp.109.152066
Actin-Binding Proteins Implicated in the Formation of the Punctate Actin Foci Stimulated by the Self-Incompatibility Response in Papaver1[W]
N. S. Poulter (2010)
10.1042/BCJ20180828
Structure of SPH (self-incompatibility protein homologue) proteins: a widespread family of small, highly stable, secreted proteins.
K. Rajasekar (2019)
10.1042/BST20130223
Interactions between pollen tube and pistil control pollen tube identity and sperm release in the Arabidopsis female gametophyte.
Alexander R Leydon (2014)
Etude des mécanismes d'adhésion des tubes polliniques d'Arabidopsis thaliana par une approche de génétique chimique
Flavien Dardelle (2011)
10.1093/mp/sst061
Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization.
T. Dresselhaus (2013)
10.1038/nplants.2016.130
Non-self- and self-recognition models in plant self-incompatibility
S. Fujii (2016)
10.1007/s13258-017-0528-5
Morphogenesis and global analysis of transcriptional profiles of Celastrus orbiculatus aril: unravelling potential genes related to aril development
Kuiling Zu (2017)
10.1016/j.cub.2010.06.038
Plant Fertilization: Bursting Pollen Tubes!
N. Franklin-Tong (2010)
10.1007/s11295-011-0403-5
Identification of marker-trait associations for self-compatibility in a segregating mapping population of Theobroma cacao L.
S. Royaert (2011)
10.1016/j.pbi.2011.07.010
Attraction of tip-growing pollen tubes by the female gametophyte.
H. Takeuchi (2011)
10.4161/psb.3.4.5152
Self-incompatibility in Papaver
S. Li (2008)
10.4161/psb.25682
Species-specific interaction of EA1 with the maize pollen tube apex
Susanne Uebler (2013)
10.1104/pp.110.167510
Reactive Oxygen Species and Nitric Oxide Mediate Actin Reorganization and Programmed Cell Death in the Self-Incompatibility Response of Papaver1[W][OA]
Katie A Wilkins (2011)
10.1111/nph.16755
Creating novel specificities in a fungal nonself recognition system by single step homologous recombination events.
J. Kämper (2020)
10.1007/s00438-010-0590-z
Positional cloning of the s haplotype determining the floral and incompatibility phenotype of the long-styled morph of distylous Turnera subulata
J. D. Labonne (2010)
10.1042/BST0380588
Self-incompatibility in Papaver: identification of the pollen S-determinant PrpS.
N. S. Poulter (2010)
10.1093/jxb/erp383
The pollen S-determinant in Papaver: comparisons with known plant receptors and protein ligand partners.
M. Wheeler (2010)
10.1038/EMBOR.2009.287
Me, myself and I. The genetics and molecular biology behind self‐incompatibility and the avoidance of inbreeding in plants
P. Hunter (2009)
10.1016/j.scienta.2020.109279
Identification of an up-accumulated polyamine oxidase 2 in pollen of self-incompatible ‘Wuzishatangju’ mandarin using comparative proteomic analysis
Yi Ren (2020)
10.1186/s12870-014-0204-8
Adaptive expansion of the maize maternally expressed gene (Meg) family involves changes in expression patterns and protein secondary structures of its members
Y. Xiong (2014)
10.1111/jeb.12219
Effects of pollen availability and the mutation bias on the fixation of mutations disabling the male specificity of self‐incompatibility
T. Tsuchimatsu (2013)
Genetic manipulation of self-incompatibility in diploid potato species
D. Dzidzienyo (2013)
10.1270/JSBBR.16.53
Current challenges for elucidating novel molecular mechanisms of self-incompatibility
Katsuyuki Kakeda (2014)
10.1093/jxb/ers108
Molecular bases and evolutionary dynamics of self-incompatibility in the Pyrinae (Rosaceae).
P. De Franceschi (2012)
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