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Self-incompatibility triggers programmed cell death in Papaver pollen

Abstract

Sexual reproduction in many angiosperm plants involves self-incompatibility (SI), which is one of the most important mechanisms to prevent inbreeding. SI is genetically controlled by the S-locus, and involves highly specific interactions during pollination between pollen and the pistil on which it lands. This results in the rejection of incompatible (‘self’) pollen, whereas compatible (‘non-self’) pollen is allowed to fertilize the plant1. In Papaver rhoeas, S-proteins encoded by the stigma component of the S-locus interact with incompatible pollen, triggering a Ca2+-dependent signalling network2,3,4,5,6,7, resulting in the inhibition of pollen-tube growth. Programmed cell death (PCD) is a mechanism used by many organisms to destroy unwanted cells in a precisely regulated manner8,9,10. Here we show that PCD is triggered by SI in an S-specific manner in incompatible pollen. This provides a demonstration of a SI system using PCD, revealing a novel mechanism to prevent self-fertilization. Furthermore, our data reveal that the response is biphasic; rapid inhibition of pollen-tube growth is followed by PCD, which is involved in a later ‘decision-making’ phase, making inhibition irreversible.

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Figure 1: DEVD permits pollen-tube growth recovery after arrest by SI.
Figure 2: SI triggers the release of cytochrome c into the cytosol of incompatible pollen tubes.
Figure 3: SI-stimulated incompatible pollen has an activity that can cleave bovine PARP.

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Acknowledgements

We thank C. Franklin and B. de Graaf for a critical reading of the manuscript. This work was funded by the BBSRC.

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Correspondence to Vernonica E. Franklin-Tong.

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Thomas, S., Franklin-Tong, V. Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305–309 (2004). https://doi.org/10.1038/nature02540

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