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Identification of the pollen self-incompatibility determinant in Papaver rhoeas

Nature volume 459, pages 992–995 (2009)Cite this article

A Corrigendum to this article was published on 02 December 2015

This article has been updated

Abstract

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 locus1,2. ‘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 death3,4,5,6,7. 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.

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Figure 1: Organization and expression of PrpS1 .
Figure 2: PrpS is pollen-membrane associated.
Figure 3: PrpS determines S-specific pollen inhibition.

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Accession codes

Primary accessions

EMBL/GenBank/DDBJ

Data deposits

PrpS1 , PrpS3 and PrpS8 sequences have been deposited in the EMBL Nucleotide Sequence Database (http://www.ebi.ac.uk/embl/) as accessions AM743176, FN178511 and AM743177.

Change history

  • 02 December 2015

    Nature 459, 992–995 (2009); doi: 10.1038/nature08027 Recently, it has come to our attention that in the left panel of Fig. 2b of this Letter, the lanes labelled S2S4 and S6S17 were duplicated. We have reviewed the original data. It seems likely that a duplicated part of the blot was placed over laneS6S17 to aid alignment of molecular mass markers and inadvertently left there.

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Acknowledgements

We thank S. Chen-Ying for contributing preliminary data and horticultural staff for growing and collecting plant material. We also thank J. Kohn for help and advice on sequence analysis, and A. Lovering and T. Hakoshima for advice regarding structural predictions. We wish to acknowledge the long-term contribution from M. Lawrence, who initiated studies on Papaver self-incompatibility. Work in the laboratories of F.C.H.F. and V.E.F.-T. is funded by the Biotechnology and Biological Sciences Research Council (BBSRC); this work was supported by grant BB/C501325/1.

Author Contributions M.J.W., B.H.J.d.G. and N.H. contributed equally to this work. F.C.H.F. and V.E.F.-T. are joint senior authors.

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Author notes

  1. Michael J. Wheeler & Barend H. J. de Graaf

    Present address: Present addresses: Warwick HRI, Wellesbourne, Warwick CV35 9EF, UK (M.J.W.); School of Biosciences, Cardiff University, Cardiff CF10 3AT, UK (B.H.J.d.G.).,

  2. Michael J. Wheeler, Barend H. J. de Graaf and Natalie Hadjiosif: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK ,

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

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Correspondence to Vernonica E. Franklin-Tong.

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Wheeler, M., de Graaf, B., Hadjiosif, N. et al. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459, 992–995 (2009). https://doi.org/10.1038/nature08027

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