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Understanding the Transcriptional Regulation of Secondary Cell Wall Biosynthesis in the Model Grass Brachypodium Distachyon

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Understanding the Transcriptional Regulation of Secondary Cell Wall Biosynthesis in the Model Grass Brachypodium Distachyon University of Massachusetts Amherst ScholarWorks@UMass Amherst Doctoral Dissertations Dissertations and Theses Summer November 2014 Understanding the transcriptional regulation of secondary cell wall biosynthesis in the model grass Brachypodium distachyon Pubudu Handakumbura University of Massachusetts Amherst Follow this and additional works at: https://scholarworks.umass.edu/dissertations_2 Part of the Biology Commons, Biotechnology Commons, Molecular Genetics Commons, and the Plant Biology Commons Recommended Citation Handakumbura, Pubudu, "Understanding the transcriptional regulation of secondary cell wall biosynthesis in the model grass Brachypodium distachyon" (2014). Doctoral Dissertations. 208. https://doi.org/10.7275/6002117.0 https://scholarworks.umass.edu/dissertations_2/208 This Open Access Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks@UMass Amherst. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact [email protected]. Understanding the transcriptional regulation of secondary cell wall biosynthesis in the model grass Brachypodium distachyon A Dissertation Presented by PUBUDU P HANDAKUMBURA Submitted to the Graduate School of the University of Massachusetts Amherst in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY September 2014 Plant Biology Graduate Program © Copyright by Pubudu P Handakumbura 2014 All Rights Reserved Understanding the transcriptional regulation of secondary cell wall biosynthesis in the model grass Brachypodium distachyon A Dissertation Presented by PUBUDU P HANDAKUMBURA Approved as to style and content by: _______________________________________ Samuel P. Hazen, Chair _______________________________________ Elsbeth L. Walker, Member _______________________________________ Magdalena Bezanilla, Member _______________________________________ John M. Lopes, Member ____________________________________ Elsbeth L. Walker, Director Plant Biology Graduate Program DEDICATION To my loving husband Rasitha. ACKNOWLEDGMENTS I would like to thank my advisor, Samuel Hazen, for his mentoring, Hazen lab members and my colleagues from the Plant Biology graduate program. I would also like to thank my family and friends for their support and encouragement throughout my graduate studies. v ABSTRACT UNDERSTANDING THE TRANSCRIPTIONAL REGULATION OF SECONDARY CELL WALL BIOSYNTHESIS IN THE MODEL GRASS Brachypodium distachyon SEPTEMBER 2014 PUBUDU P HANDAKUMBURA, B.S., UNIVERSITY OF COLOMBO, SRI LANKA Ph.D., UNIVERSITY OF MASSACHUSETTS AMHERST Directed by: Dr. Samuel P. Hazen Secondary cell wall synthesis occurs in specialized cell types following completion of cell enlargement. By virtue of mechanical strength provided by a wall thickened with cellulose, hemicelluloses, and lignin, these cells can function as water- conducting vessels and provide structural support. Several transcription factor families regulate genes encoding wall synthesis enzymes. Certain NAC and MYB proteins directly bind upstream of structural genes and other transcription factors. The most detailed model of this regulatory network is established predominantly for a eudicot, Arabidopsis thaliana. In grasses, both the patterning and the composition of secondary cell walls are distinct from that of eudicots. These differences suggest transcriptional regulation is similarly distinct. Putative rice and maize orthologs of several eudicot cell wall regulators genetically complement mutants of A. thaliana or result in wall defects when constitutively over-expressed; nevertheless, aside from maize ZmMYB31, switchgrass PvMYB4, and Brachypodium BdSWN5, function has not been tested in a grass. Similar to the seminal work conducted in A. thaliana, gene expression profiling in vi maize, rice, and other grasses implicates additional genes as regulators. Characterization of these genes in a grass species will continue to elucidate the relationship between the transcription regulatory networks of eudicots and grasses. In the context of this dissertation two cell wall genes responsible for synthesizing cellulose in the secondary cell walls were characterized. Several MYBs, a NAC and a bZIP protein was found to interact with the cellulose gene promoters. A reverse genetics approach was used to functionally characterize two of those regulators, MYB48 and GNRF. MYB48 is the first grass specific cell wall regulator found to positively regulate cell wall biosynthesis by binding to the cellulose and lignin gene promoters. It regulates above ground biomass in B. distachyon. GNRF, on the hand, unlike the characterized NAC proteins, was shown to repress cell wall biosynthesis. GNRF is also repressing flowering in B. distachyon, a novel regulatory function that has not been associated with the characterized NAC proteins to date. Further characterization of GNRF is likely to provide new insights into the pleiotropic regulatory roles of this protein. vii TABLE OF CONTENTS Page ACKNOWLEDGMENTS ...................................................................................................v ABSTRACT ....................................................................................................................... vi LIST OF TABLES ............................................................................................................ xii LIST OF FIGURES ...................................................................................................... xiiiiii CHAPTER 1. INTRODUCTION ...................................................................................................1 1.1 Plant cell walls ...................................................................................................1 1.2 Transcriptional regulation in A. thaliana ...........................................................4 1.3 Grass Cell Wall Regulators ..............................................................................10 1.4 Brachypodium distachyon: a new model system for grasses...........................13 2. PERTURBATION OF Brachypodium distachyon CELLULOSE SYNTHASE A4 OR 7 RESULTS IN ABNORMAL CELL WALLS .............................17 2.1 Introduction .....................................................................................................17 2.2 Materials and Methods .....................................................................................20 2.2.1 Plant material and growth .................................................................20 2.2.2 Identification of CELLULOSE SYNTHASE A genes ........................20 2.2.3 Measurements of transcript abundance .............................................21 2.2.4 RNA in situ hybridization .................................................................22 2.2.5 Artificial microRNA constructs ........................................................23 2.2.6 Plant transformation ..........................................................................24 2.2.7 Genomic DNA extraction and genotyping .......................................24 2.2.8 Light microscopy ..............................................................................25 2.2.9 X-ray diffraction profiles and sum-frequency-generation vibration spectroscopy .........................................................................26 viii 2.2.10 Statistical analysis ...........................................................................27 2.3 Results ..............................................................................................................27 2.3.1 Brachypodium distachyon CESA gene family ..................................27 2.3.2 Brachypodium distachyon secondary cell wall CESA gene expression ............................................................................................32 2.3.3 Localization of putative secondary cell wall CESA transcripts ........36 2.3.4 Artificial microRNAs targeting BdCESA4 and BdCESA7................36 2.3.5 BdCESA4 and BdCESA7 knock-down lines and the structure of the stem ............................................................................................39 2.3.6 Knock-down of BdCESA4 and BdCESA7 and crystalline cellulose content...................................................................................42 2.4 Discussion ........................................................................................................48 3. BdMYB48 IS A GRASS SPECIFIC POSITIVE REGULATOR OF SECONDARY CELL WALL SYNTHESIS AND BIOFUEL FEEDSTOCK ATTRIBUTES IN Brachypodium distachyon ...................................................................53 3.1 Introduction ......................................................................................................53 3.2 Materials and Methods .....................................................................................56 3.2.1 Phylogenetic analysis ........................................................................56 3.2.2 Yeast one-hybrid assay .....................................................................56 3.2.3 Plant material and growth conditions ...............................................57 3.2.4 Plasmid construction and plant transformation.................................57 3.2.5 Measurements of transcript abundance and localization ..................58 3.2.6 Microscopy .......................................................................................59 3.2.7 Acetyl bromide
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