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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 cellulose-based 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.
Highlights
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
By genetically dissecting cellulose biosynthesis in seed coat epidermal cell development, we discovered that cellulose production involving the CESA5 subunit is indispensable for mucilage attachment to the seed coat, while CESA2, CESA5, and CESA9 subunits contribute to secondary wall synthesis in epidermal seed coat cells
We examined the expression of the CESA6-related genes CESA2, CESA5, and CESA9, which were previously shown to be expressed in the Arabidopsis seed (Beeckman et al, 2002), by crossreferencing seed coat gene expression data from GENEVESTIGATOR (Zimmermann et al, 2004)
Summary
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. The transcription factor APETALA2 (AP2) is required for the differentiation of the two outer layers of the seed coat (Jofuku et al, 1994; Western et al, 2001): seeds homozygous for mutations in AP2 show altered cell shape and lack of columellae and mucilage in the seed epidermal layer (Western et al, 2001) Other transcription factors, such as TRANSPARENT TESTA GLABRA1 (TTG1), ENHANCER OF GLABRA3, TRANSPARENT TESTA8 (TT8), and TT2/MYB5, form a WD40-bHLHMYB complex that appears to regulate mucilage biosynthesis, at least in part by activating the downstream transcription factors TTG2 and GLABRA2 (Western et al, 2001; Gonzalez et al, 2009; Li et al, 2009; Huang et al, 2011). CESA6 appears to be required for the elongation of hypocotyl cells in etiolated seedlings (Fagard et al, 2000; Desprez et al, 2002) but can be partially complemented by other CESA6-related CESAs, such as CESA2, CESA5, and CESA9 (Desprez et al, 2007; Persson et al, 2007) These genes are thought to encode components of the primary cell wall cellulose biosynthetic machinery, but when mutated individually they do not result in lethality (Desprez et al, 2007). CESA9 is required for normal secondary wall synthesis in epidermal seed coat cells in Arabidopsis (Stork et al, 2010) and functions redundantly with CESA6 during pollen development (Persson et al, 2007)
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