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SIAMESE-RELATED1 imposes differentiation of stomatal lineage ground cells into pavement cells

Nature Plants volume 9, pages 1143–1153 (2023)Cite this article

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Abstract

The leaf epidermis represents a multifunctional tissue consisting of trichomes, pavement cells and stomata, the specialized cellular pores of the leaf. Pavement cells and stomata both originate from regulated divisions of stomatal lineage ground cells (SLGCs), but whereas the ontogeny of the stomata is well characterized, the genetic pathways activating pavement cell differentiation remain relatively unexplored. Here, we reveal that the cell cycle inhibitor SIAMESE-RELATED1 (SMR1) is essential for timely differentiation of SLGCs into pavement cells by terminating SLGC self-renewal potency, which depends on CYCLIN A proteins and CYCLIN-DEPENDENT KINASE B1. By controlling SLGC-to-pavement cell differentiation, SMR1 determines the ratio of pavement cells to stomata and adjusts epidermal development to suit environmental conditions. We therefore propose SMR1 as an attractive target for engineering climate-resilient plants.

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Fig. 1: SMR1 specifically controls epidermal pavement cell number.
Fig. 2: smr1 mutant pavement cells behave like SLGCs.
Fig. 3: Pavement cell division rates of smr1, cdkb1;1 ckdb1;2, smr1 cdkb1;1 cdkb1;2, cyca2;1 cyca2;3 cyca2;4 (cyca2.134) and smr1 cyca2.134 mutant leaves.
Fig. 4: Ectopic SMR1 expression triggers pavement cell differentiation of stomatal precursor cells.
Fig. 5: The smr1 mutant epidermal phenotype is not solely caused by reduced ploidy levels.
Fig. 6: Altering SMR1 levels dampens the plant’s response to drought.

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All data are available in the main text or the supplementary materials. Source data are provided with this paper.

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Acknowledgements

We thank A. Bleys for critical reading and helping in preparing the manuscript and M. Vermeersch for expertise on the drought phenotyping platform. This work was supported by grants from the Research Foundation Flanders (nos. G011420N and G010820N). I.A. and M.D. acknowledge support from a ‘Don Carlos Antonio Lopez’ by El Programa Nacional de Becas from Paraguay predoc (BECAL no. 164/2017) and a Research Foundation Flanders postdoc grant (no. 12Q7923N), respectively.

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Authors and Affiliations

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

    Marieke Dubois, Ignacio Achon, Stefanie Polyn, Rubén Tenorio Berrío, Ilse Vercauteren, Dirk Inzé & Lieven De Veylder

  2. Center for Plant Systems Biology, VIB, Gent, Belgium

    Marieke Dubois, Ignacio Achon, Stefanie Polyn, Rubén Tenorio Berrío, Ilse Vercauteren, Dirk Inzé & Lieven De Veylder

  3. School of Biosciences, University of Sheffield, Sheffield, UK

    Robert A. Brench & Julie E. Gray

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Contributions

L.D.V. supervised the project. M.D., I.A., D.I., J.E.G. and L.D.V. designed the experiments. M.D., I.A., S.P., R.T.B., R.A.B. and I.V. performed the experiments. M.D., I.A. and L.D.V. wrote and modified the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lieven De Veylder.

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Dubois, M., Achon, I., Brench, R.A. et al. SIAMESE-RELATED1 imposes differentiation of stomatal lineage ground cells into pavement cells. Nat. Plants 9, 1143–1153 (2023). https://doi.org/10.1038/s41477-023-01452-7

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