SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae

• Published in: The Plant journal : for cell and molecular biology Vol. 96; no. 3; pp. 532 - 545
• Main Authors: Handakumbura, Pubudu P., Brow, Kathryn, Whitney, Ian P., Zhao, Kangmei, Sanguinet, Karen A., Lee, Scott J., Olins, Jennifer, Romero‐Gamboa, Sandra P., Harrington, Michael J., Bascom, Carlisle J., MacKinnon, Kirk J‐M., Veling, Michael T., Liu, Lifeng, Lee, Ji E., Vogel, John P., O'Malley, Ronan C., Bezanilla, Magdalena, Bartley, Laura E., Hazen, Samuel P.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-11-2018; Society for Experimental Biology
• Subjects: Bioconversion; Biomass; Biosynthesis; Brachypodium distachyon; Brassicaceae; Cell walls; Cellulose; Cellulose fibers; Flowering; Gene expression; Genes; Grasses; Hemicellulose; Lignin; MYB transcription factor; Phenotypes; Phylogeny; Plants (botany); Promoters; Reduction; sclerenchyma cell; secondary cell wall; Synteny; Thickening; Transcription factors; Transgenic plants; Xylem; sclerenchyma cell; secondary cell wall; MYB transcription factor; Brachypodium distachyon
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14047

Summary
Grass biomass is comprised chiefly of secondary walls that surround fiber and xylem cells. A regulatory network of interacting transcription factors in part regulates cell wall thickening. We identified Brachypodium distachyon SECONDARY WALL ASSOCIATED MYB1 (SWAM1) as a potential regulator of secondary cell wall biosynthesis based on gene expression, phylogeny, and transgenic plant phenotypes. SWAM1 interacts with cellulose and lignin gene promoters with preferential binding to AC‐rich sequence motifs commonly found in the promoters of cell wall‐related genes. SWAM1 overexpression (SWAM‐OE) lines had greater above‐ground biomass with only a slight change in flowering time while SWAM1 dominant repressor (SWAM1‐DR) plants were severely dwarfed with a striking reduction in lignin of sclerenchyma fibers and stem epidermal cell length. Cellulose, hemicellulose, and lignin genes were significantly down‐regulated in SWAM1‐DR plants and up‐regulated in SWAM1‐OE plants. There was no reduction in bioconversion yield in SWAM1‐OE lines; however, it was significantly increased for SWAM1‐DR samples. Phylogenetic and syntenic analyses strongly suggest that the SWAM1 clade was present in the last common ancestor between eudicots and grasses, but is not in the Brassicaceae. Collectively, these data suggest that SWAM1 is a transcriptional activator of secondary cell wall thickening and biomass accumulation in B. distachyon.
Significance Statement
Feed‐forward transcription regulatory loops activate the thickening of secondary cell walls in Arabidopsis thaliana. Here we report on the MYB transcription SWAM1, which is present in grasses and many eudicotyledons, but not the Brassicaceae. It directly activates grass cell wall biosynthesis and transgenic lines exhibit rather striking and agronomically important phenotypes.