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Organization and Expression of the GSK3/Shaggy Kinase Gene Family in the Moss Physcomitrella patens Suggest Early Gene Multiplication in Land Plants and an Ancestral Response to Osmotic Stress

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Abstract

GSK3/Shaggy kinases are involved in a wide range of fundamental processes in animal development and metabolism. In angiosperm plants, these kinases are encoded by moderate-sized gene families, which appear to have a complex set of functions. Here, we present the characterization of five members of the GSK3/Shaggy gene family in the bryophyte Physcomitrella patens. The P. patens GSK3/Shaggy kinases (PpSK) are organized in a group of closely related paralogues with respect to their gene sequence and structure. Indeed, a phylogenetic analysis of the GSK3/Shaggy kinase sequences from plants and animals showed that the five PpSK proteins are monophyletic, and closer to subgroups I and IV described in angiosperms. Expression analyses performed by quantitative real-time RT-PCR on a wide range of growing conditions showed that PpSK genes responded only to either desiccation, PEG or sorbitol. As demonstrated by both inductions of marker genes and protonemal cell plasmolyses, these treatments resulted in a hyperosmotic stress. Altogether, these data suggest that (1) GSK3/Shaggy kinase gene multiplication occurred early in plant evolution, before the separation between bryophytes and vascular plants, and (2) both gene loss and duplication occurred in the ancestor of P. patens along with functional gene diversification in angiosperms. However, conservation of the transcriptional responses between Physcomitrella and Arabidopsis suggests the identification of an ancestral response of the GSK3/Shaggy kinases genes to osmotic stress.

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Acknowledgments

We are grateful to the Moss Technology Laboratory at the University of Leeds (U.K.) for providing us with a Physcomitrella patens cDNA library and the cDNA corresponding to the EST BI741214. We thank Y. Kamisugi (University of Leeds, U.K.) for helpful discussions and advice on P. patens culture, E. Douzery (University Montpellier II) for assistance with the SH test, and Y. Henry (IBP, University Orsay, France) for help with the kinase sequence analyses. H.I. McKhann and T. Tranbarger are acknowledged for critical reading of the manuscript and M. Kreis and A. Lecharny for their intellectual support of the project.

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  1. Odile Richard

    Present address: Laboratoire de Biologie et Physiologie Moléculaire des Plantes (UMR 5004), Université Montpellier II, Place Eugène Bataillon, 34095, Montpellier Ceded 5, France

  2. Bénédicte Charrier

    Present address: UMR 7139, CNRS-UPMC-Station biologique, Place georges Teissier, 1BP74, 29682, Roscoff cedex, France

Authors and Affiliations

  1. Institut de Biotechnologie des Plantes, Bât. 630, UMR CNRS 8618, Université Paris-Sud, 91405, Orsay Cedex, France

    Odile Richard, Nicolas Paquet, Elise Haudecoeur & Bénédicte Charrier

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  1. Odile Richard
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Correspondence to Bénédicte Charrier.

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[Reviewing Editor: Nicolas Galtier]

GenBank accession numbers of P. patens GSK3/Shaggy kinases: cDNA PpSK1, AY339065; PpSK2, AY339066; PpSK3, AY339067; PpSK4, AY339068; PpSK5, AY339069. Genes: PpSK1, AY339070; PpSK2, AY339071; PpSK3, AY339072.

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Richard, O., Paquet, N., Haudecoeur, E. et al. Organization and Expression of the GSK3/Shaggy Kinase Gene Family in the Moss Physcomitrella patens Suggest Early Gene Multiplication in Land Plants and an Ancestral Response to Osmotic Stress. J Mol Evol 61, 99–113 (2005). https://doi.org/10.1007/s00239-004-0302-6

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