Abstract
The Arabidopsis (Arabidopsis thaliana) trichome birefringence (tbr) mutant has severely reduced crystalline cellulose in trichomes, but the molecular nature of TBR was unknown. We determined TBR to belong to the plant-specific DUF231 domain gene family comprising 46 members of unknown function in Arabidopsis. The genes harbor another plant-specific domain, called the TBL domain, which contains a conserved GDSL motif known from some esterases/lipases. TBR and TBR-like3 (TBL3) are transcriptionally coordinated with primary and secondary CELLULOSE SYNTHASE (CESA) genes, respectively. The tbr and tbl3 mutants hold lower levels of crystalline cellulose and have altered pectin composition in trichomes and stems, respectively, tissues generally thought to contain mainly secondary wall crystalline cellulose. In contrast, primary wall cellulose levels remain unchanged in both mutants as measured in etiolated tbr and tbl3 hypocotyls, while the amount of esterified pectins is reduced and pectin methylesterase activity is increased in this tissue. Furthermore, etiolated tbr hypocotyls have reduced length with swollen epidermal cells, a phenotype characteristic for primary cesa mutants or the wild type treated with cellulose synthesis inhibitors. Taken together, we show that two TBL genes contribute to the synthesis and deposition of secondary wall cellulose, presumably by influencing the esterification state of pectic polymers.
Highlights
The Arabidopsis (Arabidopsis thaliana) trichome birefringence mutant has severely reduced crystalline cellulose in trichomes, but the molecular nature of TRICHOME BIREFRINGENCE (TBR) was unknown
Mutant seedlings frequently displayed a marked reduction in hypocotyl length (Fig. 2A), reminiscent of etiolated primary cesa mutant seedlings like prc1-8, ixr12, and rsw1-10 (Fagard et al, 2000; Mouille et al, 2003) and dark-grown wild-type seedlings treated with cellulose synthesis inhibitors like thaxtomin A (Scheible et al, 2003; Bischoff et al, 2009) or dichlobenil (Robert et al, 2004)
Such symptoms were never observed in wild-type seedlings (Fig. 2D). These results point to a function of TBR in primary cell wall synthesis in etiolated seedlings. To assess whether this is due to reduced levels of primary wall cellulose, we measured the amount of crystalline cellulose in tbr and wild-type hypocotyls (Fig. 2E)
Summary
The Arabidopsis (Arabidopsis thaliana) trichome birefringence (tbr) mutant has severely reduced crystalline cellulose in trichomes, but the molecular nature of TBR was unknown. Analysis of Arabidopsis fragile fiber (fra) mutants, in which interfascicular fibers exhibit reduced mechanical strength, resulted in the identification of mutant alleles for the secondary CESA genes (fra and fra; Zhong et al, 2003) and yielded novel components, some of which presumably are indirectly required for secondary wall synthesis These include the kinesin-like protein FRA1, which is essential for oriented deposition of cellulose microfibrils and cell wall strength (Zhong et al, 2002), the katanin-like protein FRA2 involved in regulating microtubule disassembly by severing microtubules (Burk et al, 2001), a type II inositol polyphosphate 5-phosphatase (Zhong and Ye, 2004), and the GTP-binding protein RHD3 (Wang et al, 1997; Hu et al, 2003), both required for actin organization in fiber cells. IRX8 (AT5G54690) and IRX9 (AT2G37090) encode putative glycosyl transferase genes from the GT8 and GT43 families, respectively (www.cazy.org), and were found to be involved in glucuroxylan (GX) synthesis (Bauer et al, 2006; Pena et al, 2007; Persson et al, 2007), suggesting a requirement for normal hemicellulosic polysaccharide synthesis in order for normal secondary wall synthesis and cellulose deposition to occur
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