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Dynamic analysis of epidermal cell divisions identifies specific roles for COP10 in Arabidopsis stomatal lineage development

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Abstract

Stomatal development in Arabidopsis thaliana has been linked to photoreceptor-perceived light through several components of the photomorphogenic switch, whose lack of function is often seedling-lethal. CONSTITUTIVE PHOTOMORPHOGENIC 10 (COP10) is an important component of this switch, its loss of function producing stomatal clusters. Exploiting the reduced lethality of the cop10-1 mutant we characterized the developmental basis of its stomatal phenotype. Constitutive, light-independent stomata overproduction accounts for half of cop10-1 stomatal abundance and appears very early in development. Clusters are responsible for the remaining stomata excess and build-up progressively at later stages. Serial impressions of living cotyledon epidermis allowed a dynamic, quantitative analysis of stomatal lineage types by reconstructing their division histories. We found that COP10 adjusts the initiation frequency and extension of stomatal lineages (entry and amplifying asymmetric divisions) and represses stomatal fate in lineage cells; COP10 also supervises the orientation of spacing divisions in satellite lineages, preventing the appearance of stomata in contact. Aberrant accumulation of the proliferating stomatal lineage cell marker TMMpro::TMM-GFP showed that the abundant cop10-1 stomatal lineages maintained extended and ectopic competence for stomatal fate. Expression of stomatal development master genes suggests that the mutant does not bypass major molecular actors in this process. cop10-1 first leaf produces trichomes and apparently normal pavement cells, but functionally and morphologically aberrant stomata; COP10 operates genetically in parallel to the stomatal repressor SDD1 and does not generally affect epidermal cell differentiation, but seems to operate on stomatal lineages where it controls specific cell-lineage and cell-signaling developmental mechanisms.

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Abbreviations

M:

Meristemoid

MMC:

Meristemoid mother cells

GMC:

Guard mother cell

SLGC:

Stomatal-lineage ground cells

TMM :

TOO MANY MOUTHS

Ws:

Wassilewskija

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Acknowledgments

The authors thank Dr. Fred Sack (University of British Columbia, Canada) for the kind gift of the proTMM::TMM-GFP seeds, and the Nottingham Arabidopsis Stock Centre (UK) for providing cop10-1 and Ws seeds. We also thank two anonymous reviewers and the Editor for their useful criticisms during the revision of the manuscript. This work was supported by grants from the Ministerio de Ciencia e Innovación (BIO2007-60276 to C.F. and M.M., and CSD2007-00057 to C.F.) and the Consejería de Ciencia y Educación-JCCM (PAI07-0036-3278 to M.M.). IB was funded by a postdoctoral fellowship granted by the Consejería de Ciencia y Educación-JCCM.

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Authors and Affiliations

  1. Facultad de Ciencias Ambientales y Bioquímica, Universidad de Castilla-la Mancha, Avda. Carlos III s/n, 45071, Toledo, Spain

    Dolores Delgado, Isabel Ballesteros, Javier Torres-Contreras, Montaña Mena & Carmen Fenoll

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  1. Dolores Delgado
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  2. Isabel Ballesteros
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  3. Javier Torres-Contreras
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  4. Montaña Mena
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  5. Carmen Fenoll
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Corresponding authors

Correspondence to Montaña Mena or Carmen Fenoll.

Additional information

D. Delgado and I. Ballesteros contributed equally to this work.

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Delgado, D., Ballesteros, I., Torres-Contreras, J. et al. Dynamic analysis of epidermal cell divisions identifies specific roles for COP10 in Arabidopsis stomatal lineage development. Planta 236, 447–461 (2012). https://doi.org/10.1007/s00425-012-1617-y

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