Abstract
Despite a strict conservation of the vascular tissues in vascular plants (tracheophytes), our understanding of the genetic basis underlying the differentiation of secondary cell wall-containing cells in the xylem of tracheophytes is still far from complete. Using coexpression analysis and phylogenetic conservation across sequenced tracheophyte genomes, we identified a number of Arabidopsis (Arabidopsis thaliana) genes of unknown function whose expression is correlated with secondary cell wall deposition. Among these, the Arabidopsis VASCULAR-RELATED UNKNOWN PROTEIN1 (VUP1) gene encodes a predicted protein of 24 kD with no annotated functional domains but containing domains that are highly conserved in tracheophytes. Here, we show that the VUP1 expression pattern, determined by promoter-β-glucuronidase reporter gene expression, is associated with vascular tissues, while vup1 loss-of-function mutants exhibit collapsed morphology of xylem vessel cells. Constitutive overexpression of VUP1 caused dramatic and pleiotropic developmental defects, including severe dwarfism, dark green leaves, reduced apical dominance, and altered photomorphogenesis, resembling brassinosteroid-deficient mutants. Constitutive overexpression of VUP homologs from multiple tracheophyte species induced similar defects. Whole-genome transcriptome analysis revealed that overexpression of VUP1 represses the expression of many brassinosteroid- and auxin-responsive genes. Additionally, deletion constructs and site-directed mutagenesis were used to identify critical domains and amino acids required for VUP1 function. Altogether, our data suggest a conserved role for VUP1 in regulating secondary wall formation during vascular development by tissue- or cell-specific modulation of hormone signaling pathways.
Highlights
Despite a strict conservation of the vascular tissues in vascular plants, our understanding of the genetic basis underlying the differentiation of secondary cell wall-containing cells in the xylem of tracheophytes is still far from complete
Analysis of genes coexpressed with the cellulose biosynthesis genes IRX5/CELLULOSE SYNTHASE4 (CESA4), IRX3/CESA7, and IRX1/CESA8, marker genes for secondary cell wall deposition (Brown et al, 2005; Persson et al, 2005), led to the discovery of new genes required for this process, including IRX7/FRAGILE FIBER8, IRX8, IRX9, IRX14, IRX10, IRX10-LIKE (IRX10L), PARVUS, IRX15, and IRX15L (Zhong et al, 2005; Brown et al, 2007, 2009, 2011; Lee et al, 2007; Peña et al, 2007; Persson et al, 2007; Wu et al, 2009; Jensen et al, 2011)
We first selected about 200 genes strongly coregulated (r2 . 0.7 in the BioArray Resource for Plant Biology Expression Angler; Toufighi et al, 2005) with three genes known for their roles in secondary cell wall formation: CESA8, encoding a secondary cell wall-specific cellulose synthase subunit (Turner and Somerville, 1997); KNOTTED-LIKE HOMEOBOX OF ARABIDOPSIS THALIANA7, a transcriptional regulator of secondary cell wall formation (Brown et al, 2005; Li et al, 2012); and HYDROXYCINNAMOYL-COENZYME A SHIKIMATE/QUINATE HYDROXYCINNAMOYL TRANSFERASE, encoding an enzyme required for lignin biosynthesis (Hoffmann et al, 2004)
Summary
Despite a strict conservation of the vascular tissues in vascular plants (tracheophytes), our understanding of the genetic basis underlying the differentiation of secondary cell wall-containing cells in the xylem of tracheophytes is still far from complete. Using coexpression analysis and phylogenetic conservation across sequenced tracheophyte genomes, we identified a number of Arabidopsis (Arabidopsis thaliana) genes of unknown function whose expression is correlated with secondary cell wall deposition. Previous studies have identified many genes of unknown function that are tightly coexpressed with secondary cell wall-related genes (Brown et al, 2005; Persson et al, 2005; Oikawa et al, 2010), suggesting that potentially novel functions are involved in vascular development or secondary cell wall formation
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