The Sterol Methyltransferases SMT1, SMT2, and SMT3 Influence Arabidopsis Development through Nonbrassinosteroid Products    

Abstract

Plant sterols are structural components of cell membranes that provide rigidity, permeability, and regional identity to membranes. Sterols are also the precursors to the brassinosteroid signaling molecules. Evidence is accumulating that specific sterols have roles in pattern formation during development. COTYLEDON VASCULAR PATTERNING1 (CVP1) encodes C-24 STEROL METHYLTRANSFERASE2 (SMT2), one of three SMTs in Arabidopsis (Arabidopsis thaliana). SMT2 and SMT3, which also encodes a C-24 SMT, catalyze the reaction that distinguishes the synthesis of structural sterols from signaling brassinosteroid derivatives and are highly regulated. The deficiency of SMT2 in the cvp1 mutant results in moderate developmental defects, including aberrant cotyledon vein patterning, serrated floral organs, and reduced stature, but plants are viable, suggesting that SMT3 activity can substitute for the loss of SMT2. To test the distinct developmental roles of SMT2 and SMT3, we identified a transcript null smt3 mutant. Although smt3 single mutants appear wild type, cvp1 smt3 double mutants show enhanced defects relative to cvp1 mutants, such as discontinuous cotyledon vein pattern, and produce novel phenotypes, including defective root growth, loss of apical dominance, sterility, and homeotic floral transformations. These phenotypes are correlated with major alterations in the profiles of specific sterols but without significant alterations to brassinosteroid profiles. The alterations to sterol profiles in cvp1 mutants affect auxin response, demonstrated by weak auxin insensitivity, enhanced axr1 auxin resistance, ectopically expressed DR5:b-glucuronidase in developing embryos, and defective response to auxin-inhibited PIN2-green fluorescent protein endocytosis. We discuss the developmental roles of sterols implied by these results.

Sterol and genomic analyses validate the sponge biomarker hypothesis

“…This finding is consistent with evidence for multiple rounds of whole-genome duplication in plants and is recapitulated in the high plant paralog counts for all genes we analyzed (Supporting Information). The overabundance of plant SMTs suggests that they exhibit overlapping functions that are not necessarily related to sterol synthesis, a hypothesis supported by evidence from Arabidopsis thaliana (22). However, the tight correlation holds for the rest of the bikonts, including a unique third SMT in the pelagophyte A. anophagefferens.…”

Sterol Methyl Oxidases Affect Embryo Development via Auxin-Associated Mechanisms

“…On the one hand, the expression of sterol biosynthetic pathway genes such as FK was up-regulated by auxin (He et al, 2003), concentrations of the major plant sterols were significantly reduced in the axr1-12 auxin signaling mutant (Pan et al, 2009), and sterol mutants such as fk and cvp1 displayed altered responses to auxin (Souter et al, 2002;Carland et al, 2010). On the other hand, sterols were required for auxin signaling and polar transportation.…”

“…1). Although previous studies did not observe endosperm developmental defects in upstream sterol mutants, they found cell division defects in embryos and roots (Schrick et al, 2000;Souter et al, 2002;Carland et al, 2010). Detailed analyses of endosperm development in those upstream mutants will clarify whether the endosperm nuclear proliferation defects are specific to the smo2-1 smo2-2 double mutant.…”

“…Further analysis showed that steroldependent endocytosis was required for the postcytokinetic establishment of PIN2 polarity (Men et al, 2008). Additionally, sterols were found to be essential for auxin-inhibited PIN2 protein endocytosis (Pan et al, 2009;Carland et al, 2010). A previous study found that sterols also are required for the trans-Golgi networkto-plasma membrane trafficking of the ATP-binding cassette B19 auxin transporter (Yang et al, 2013).…”

“…Sterols were found to have intimate interactions with plant hormones, such as auxin and ethylene. Polar auxin transport (PAT) or auxin response was hindered in sterol biosynthetic mutants (Willemsen et al, 2003;Men et al, 2008;Carland et al, 2010;Pullen et al, 2010). Inhibition of ethylene biosynthesis or signaling partially rescued fk, hyd1, and cyp51A2 mutants (Kim et al, 2010;Pullen et al, 2010).…”