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

Abstract

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.

Authors:
 [1];  [2];  [3];  [4];  [5];  [1];  [2];  [1];  [2];  [1];  [3];  [2];  [6];  [6];  [6];  [6];  [2];  [4];  [2]
  1. Biology Department, University of Massachusetts, Amherst MA 01003 USA; Plant Biology Graduate Program, University of Massachusetts, Amherst MA 01003 USA
  2. Biology Department, University of Massachusetts, Amherst MA 01003 USA
  3. Biology Department, University of Massachusetts, Amherst MA 01003 USA; Molecular and Cellular Biology Graduate Program, University of Massachusetts, Amherst MA 01003 USA
  4. Department of Microbiology and Plant Biology, University of Oklahoma, Norman OK 73019 USA
  5. Department of Crop and Soil Sciences, Washington State University, Pullman WA 99164 USA
  6. DOE Joint Genome Institute, Walnut Creek CA 94598 USA
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory-National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1529122
DOE Contract Number:  
FG02-08ER64700; SC0006641; SC006904; AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 96; Journal Issue: 3; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English

Citation Formats

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., and Hazen, Samuel P. SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae. United States: N. p., 2018. Web. doi:10.1111/tpj.14047.
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. SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae. United States. doi:10.1111/tpj.14047.
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., and Hazen, Samuel P. Wed . "SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae". United States. doi:10.1111/tpj.14047.
@article{osti_1529122,
title = {SECONDARY WALL ASSOCIATED MYB1 is a positive regulator of secondary cell wall thickening in Brachypodium distachyon and is not found in the Brassicaceae},
author = {Handakumbura, Pubudu P. and Brow, Kathryn and Whitney, Ian P. and Zhao, Kangmei and Sanguinet, Karen A. and Lee, Scott J. and Olins, Jennifer and Romero-Gamboa, Sandra P. and Harrington, Michael J. and Bascom, Carlisle J. and MacKinnon, Kirk J-M. and Veling, Michael T. and Liu, Lifeng and Lee, Ji E. and Vogel, John P. and O'Malley, Ronan C. and Bezanilla, Magdalena and Bartley, Laura E. and Hazen, Samuel P.},
abstractNote = {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.},
doi = {10.1111/tpj.14047},
journal = {The Plant Journal},
issn = {0960-7412},
number = 3,
volume = 96,
place = {United States},
year = {2018},
month = {9}
}

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