TY - JOUR
T1 - Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment
AU - Mendu, Venugopal
AU - Griffiths, Jonathan S.
AU - Persson, Staffan
AU - Stork, Jozsef
AU - Bruce Downie, A.
AU - Voiniciuc, Cǎtǎlin
AU - Haughn, George W.
AU - de Bolt, Seth
N1 - 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.
PY - 2011/9
Y1 - 2011/9
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=80052406577&partnerID=8YFLogxK
U2 - 10.1104/pp.111.179069
DO - 10.1104/pp.111.179069
M3 - Article
C2 - 21750228
AN - SCOPUS:80052406577
SN - 0032-0889
VL - 157
SP - 441
EP - 453
JO - Plant physiology
JF - Plant physiology
IS - 1
ER -