Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment

Venugopal Mendu, Jonathan S. Griffiths, Staffan Persson, Jozsef Stork, A. Bruce Downie, Cǎtǎlin Voiniciuc, George W. Haughn, Seth de Bolt

Research output: Contribution to journalArticlepeer-review

119 Scopus citations

Abstract

Arabidopsis (Arabidopsis thaliana) epidermal seed coat cells follow a complex developmental program where, following fertilization, cells of the ovule outer integument differentiate into a unique cell type. Two hallmarks of these cells are the production of a doughnut-shaped apoplastic pocket filled with pectinaceous mucilage and the columella, a thick secondary cell wall. Cellulose is thought to be a key component of both these secondary cell wall processes. Here, we investigated the role of cellulose synthase (CESA) subunits CESA2, CESA5, and CESA9 in the seed coat epidermis. We characterized the roles of these CESA proteins in the seed coat by analyzing cell wall composition and morphology in cesa mutant lines. Mutations in any one of these three genes resulted in lower cellulose content, a loss of cell shape uniformity, and reduced radial wall integrity. In addition, we found that attachment of the mucilage halo to the parent seed following extrusion is maintained by cellulosebased connections requiring CESA5. Hence, we show that cellulose fulfills an adhesion role between the extracellular mucilage matrix and the parent cell in seed coat epidermal cells. We propose that mucilage remains attached to the seed coat through interactions between components in the seed mucilage and cellulose. Our data suggest that CESA2 and CESA9 serve in radial wall reinforcement, as does CESA5, but CESA5 also functions in mucilage biosynthesis. These data suggest unique roles for different CESA subunits in one cell type and illustrate a complex role for cellulose biosynthesis in plant developmental biology.

Original languageEnglish
Pages (from-to)441-453
Number of pages13
JournalPlant Physiology
Volume157
Issue number1
DOIs
StatePublished - Sep 2011

Bibliographical note

Funding Information:
Acknowledgements This study was supported by the Medical Research Council of Canada (MT-11876) and Heart and Stroke Foundation of Quebec. Chantale Simard is the recipient of a s tu-dentship from the Fonds pour la Formation de Chercheurs et l'Aide aÁ la Recherche (FCAR) and MDS Pharma Services. Jacques Turgeon was the recipient of a scholarship from the Joseph C. Edwards Foundation. The authors als o thank Michel Blouin, for technical assistance, Josée Morin for stastistical analysis and Vicky Falardeau and Nicole Garneau for nursing care. The study as desc ribed in this article complies fully with the current laws regarding experiments involving humans in Canada.

Funding

FundersFunder number
National Science Foundation (NSF)0937657

    ASJC Scopus subject areas

    • Physiology
    • Genetics
    • Plant Science

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