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KIRA1 and ORESARA1 terminate flower receptivity by promoting cell death in the stigma of Arabidopsis

Nature Plants volume 4, pages 365–375 (2018)Cite this article

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Abstract

Flowers have a species-specific functional life span that determines the time window in which pollination, fertilization and seed set can occur. The stigma tissue plays a key role in flower receptivity by intercepting pollen and initiating pollen tube growth toward the ovary. In this article, we show that a developmentally controlled cell death programme terminates the functional life span of stigma cells in Arabidopsis. We identified the leaf senescence regulator ORESARA1 (also known as ANAC092) and the previously uncharacterized KIRA1 (also known as ANAC074) as partially redundant transcription factors that modulate stigma longevity by controlling the expression of programmed cell death–associated genes. KIRA1 expression is sufficient to induce cell death and terminate floral receptivity, whereas lack of both KIRA1 and ORESARA1 substantially increases stigma life span. Surprisingly, the extension of stigma longevity is accompanied by only a moderate extension of flower receptivity, suggesting that additional processes participate in the control of the flower’s receptive life span.

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Fig. 1: Stigma degeneration is a developmentally timed process correlated with loss of floral receptivity.
Fig. 2: Ageing unpollinated papilla cells die in a dPCD-like process.
Fig. 3: KIR1 and ORE1 are upregulated in senescent papilla cells.
Fig. 4: ORE1 and KIR1 redundantly control stigma life span.
Fig. 5: Overexpression of ORE1 and KIR1 induces senescence and cell death symptoms to varying degrees.
Fig. 6: ORE1 and KIR1 homodimers and heterodimers directly control expression of dPCD-associated genes.
Fig. 7: Loss of KIR1 and ORE1 function moderately extends seed set in aged flowers.

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Acknowledgements

We thank the members of the PCD laboratory for discussions and critical feedback on the manuscript, V. Storme for assistance with statistical analysis, and A. Bleys for help with preparing the manuscript. We gratefully acknowledge funding from the Chinese Scholarship Council (CSC; project number 201206910025 to Z.G.), the Fonds Wetenschappelijk Onderzoek (FWO; project number G005112N to A.D.; fellowship number 12I7417N to Z.L.), the Belgian Federal Science Policy Office (BELSPO; to Y.S.), the Agency for Innovation by Science and Technology of Belgium (IWT; fellowship number 121110 to M.V.D.), the Hercules foundation (grant AUGE-09-029 to K.D.), and the ERC StG PROCELLDEATH (project number 639234 to M.K.N.).

Author information

Author notes

  1. Zhen Gao

    Present address: Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China

  2. Yuliya Salanenka

    Present address: Institute of Science and Technology (IST), Klosterneuburg, Austria

  3. These authors contributed equally: Zhen Gao, Anna Daneva.

Authors and Affiliations

  1. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

    Zhen Gao, Anna Daneva, Yuliya Salanenka, Matthias Van Durme, Marlies Huysmans, Zongcheng Lin, Freya De Winter, Steffen Vanneste, Mansour Karimi, Jan Van de Velde, Klaas Vandepoele & Moritz K. Nowack

  2. VIB Center of Plant Systems Biology, Ghent, Belgium

    Zhen Gao, Anna Daneva, Yuliya Salanenka, Matthias Van Durme, Marlies Huysmans, Zongcheng Lin, Freya De Winter, Steffen Vanneste, Mansour Karimi, Jan Van de Velde, Klaas Vandepoele & Moritz K. Nowack

  3. Lab of Plant Growth Analysis, Ghent University Global Campus, Yeonsu-gu, Incheon, Republic of Korea

    Steffen Vanneste

  4. Laboratory of Food Technology and Engineering, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

    Davy Van de Walle & Koen Dewettinck

  5. VIB Center for Inflammation Research, Ghent, Belgium

    Bart N. Lambrecht

  6. Department of Internal Medicine, Ghent University, Ghent, Belgium

    Bart N. Lambrecht

  7. Department of Pulmonary Medicine, Ersamus MC, Rotterdam, the Netherlands

    Bart N. Lambrecht

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Contributions

Z.G. and A.D., designed and performed most of the experiments. Y.S. initiated the project and performed experiments. M.V.D., M.H., Z.L., F.D.W., S.V. and M.K. performed experiments, analysed the data and interpreted the results. J.V.d.V. and K.V. performed TF binding site predictions. D.V.d.W. and K.D. contributed to the cryo-scanning electron microscopy experiments, and B.N.L. contributed to the setup of stigma live-cell imaging. M.K.N. supervised the project and designed the experiments. Z.G., A.D. and M.K.N. wrote the manuscript.

Corresponding author

Correspondence to Moritz K. Nowack.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7, Supplementary References, Supplementary Table 2 and Supplementary Methods

Reporting Summary

Supplementary Table 1

Cluster analysis of differentially expressed genes identified by RNA sequencing of developmental stigma series.

Supplementary Table 3

A table of all primers used in this study.

Supplementary Video 1

Macroscopic phenotyping of an unpollinated stigma life span with an SLR camera.

Supplementary Video 2

Macroscopic phenotyping of an unpollinated stigma life span with the webcam system.

Supplementary Video 3

Microscopic imaging of stigmatic papilla cell death.

Supplementary Video 4

Microscopic imaging of stigmatic papilla cells dying in clusters.

Supplementary Video 5

Microscopic imaging of cell death events taking place in dying papilla cell.

Supplementary Video 6

ORE1 and KIR1 mutants show extended papilla life spans.

Supplementary Video 7

Induced overexpression of KIR1 and ORE1 leads to growth arrest and death of entire seedlings.

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Gao, Z., Daneva, A., Salanenka, Y. et al. KIRA1 and ORESARA1 terminate flower receptivity by promoting cell death in the stigma of Arabidopsis. Nature Plants 4, 365–375 (2018). https://doi.org/10.1038/s41477-018-0160-7

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