Degradation of glyoxalase I in Brassica napus stigma leads to self-incompatibility response

Abstract

Self-incompatibility (rejection of ‘self’-pollen) is a reproductive barrier that allows hermaphroditic flowering plants to prevent inbreeding, to promote outcrossing and hybrid vigour. The self-incompatibility response in Brassica involves allele-specific interaction between the pollen small cysteine-rich, secreted protein ligand (SCR/SP11) and the stigmatic S-receptor kinase (SRK), which leads to the activation of the E3 ubiquitin ligase ARC1 (Armadillo repeat-containing 1), resulting in proteasomal degradation of compatibility factors needed for successful pollination. Despite this, targets of ARC1 and the intracellular signalling network that is regulated by these targets, have remained elusive. Here we show that glyoxalase I (GLO1), an enzyme that is required for the detoxification of methylglyoxal (MG, a cytotoxic by-product of glycolysis), is a stigmatic compatibility factor required for pollination to occur and is targeted by the self-incompatibility system. Suppression of GLO1 was sufficient to reduce compatibility, and overexpression of GLO1 in self-incompatible Brassica napus stigmas resulted in partial breakdown of the self-incompatibility response. ARC1-mediated destruction of GLO1 after self-pollination results in increased MG levels and a concomitant increase in MG-modified proteins (including GLO1), which are efficiently targeted for destruction in the papillary cells, leading to pollen rejection. Our findings demonstrate the elegant nature of plants to use a metabolic by-product to regulate the self-incompatibility response.

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Figure 1: GLO1 is required for compatible pollination.
Figure 2: GLO1 is a target of ARC1 during self-incompatibility.
Figure 3: GLO1 overexpression in self-incompatible W1 stigmas leads to partial breakdown of the self-incompatibility response.
Figure 4: GLO1 is modified by MG in vivo and MG-modified GLO1 is efficiently ubiquitinated by ARC1.
Figure 5

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Acknowledgements

We thank Dr Douglas Muench for the epi-fluorescence microscope facility and Dr Andre Buret for the microplate reader. We also thank Dr Daphne Goring for ARC1 antisense transgenic lines. This work was supported by the Natural Sciences and Engineering Research Council of Canada grants and start-up funds from the University of Calgary to M.A.S.

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S.S. and M.A.S. conceived and initiated the project. S.S. and M.A.S. designed the research; S.S. performed all the experiments, and M.J. was responsible for analysis of subcellular localization of GLO1 and confocal microscopy; S.S., M.J. and M.A.S. analysed the data; S.S. and M.A.S. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Marcus A. Samuel.

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The authors declare no competing financial interests.

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Sankaranarayanan, S., Jamshed, M. & Samuel, M. Degradation of glyoxalase I in Brassica napus stigma leads to self-incompatibility response. Nature Plants 1, 15185 (2015). https://doi.org/10.1038/nplants.2015.185

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