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Functional Characterization of R2R3-MYB Activators and Repressors As Flavonoid Transcriptional Regulators in Poplar

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Functional Characterization of R2R3-MYB Activators and Repressors As Flavonoid Transcriptional Regulators in Poplar Functional Characterization of R2R3-MYB Activators and Repressors as Flavonoid Transcriptional Regulators in Poplar by Dawei Ma B.Sc., Fudan University, 2012 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in the Department of Biology ã Dawei Ma, 2019 University of Victoria All rights reserved. This Dissertation may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii Supervisory Committee Functional Characterization of R2R3-MYB Activators and Repressors as Flavonoid Transcriptional Regulators in Poplar by Dawei Ma B.Sc., Fudan University, 2012 Supervisory Committee Dr. C. Peter Constabel, Supervisor Department of Biology Dr. Jürgen Ehlting, Departmental member Department of Biology Dr. Armand Séguin, Departmental Member Department of Biology Dr. Chris Nelson, Outside Member Department of Biochemistry iii Abstract Flavonoids are important and ubiquitous secondary metabolites and are known to participate in various developmental and stress response processes in plants. Common flavonoids include anthocyanins, proanthocyanidins and flavonols. This thesis aims to determine, at the molecular level, how the biosynthesis of flavonoids, in particular the proanthocyanidins, is regulated in poplar. Poplars accumulate large amount of flavonoids and the major flavonoid biosynthetic genes in poplar have been identified. Flavonoid biosynthesis is known to be regulated by MYB transcription factors. Previous work had identified MYB134 as a key regulator of proanthocyanidin synthesis in poplar. Here I describe experiments on five additional genes encoding MYB activators (MYB115 and MYB117), MYB repressors (MYB165 and MYB194), and one bHLH cofactor (bHLH131) as possible flavonoid regulators in poplar. The objective of this work is to determine the in planta functions of these new flavonoid regulators using reverse genetic methods, phytochemical and transcriptome analysis, to identify their target genes and to determine how these transcriptional regulators interact using promoter transactivation and yeast two- hybrid assays. MYB115 was identified as a second proanthocyanidin regulator. Similar to the effects of MYB134, overexpression of MYB115 in poplar led to increased proanthocyanidin content and upregulated flavonoid biosynthesis genes, but reduced the accumulation of salicinoids. Overexpression of repressor type MYBs, MYB165 or MYB194 led to reduced anthocyanin, salicinoid and hydroxycinnamic ester accumulation in leaves, while reducing proanthocyanidin content in roots. Transcriptome analysis demonstrated the downregulation of most flavonoid genes in these transgenics, as well as some shikimate pathway genes, confirming the broad repression function on the phenylpropanoid pathway. By contrast, MYB117 encodes an anthocyanin activator, and was shown to be specific to this branch of the flavonoid pathway. Overexpression of MYB117 in transgenic poplar increased accumulation of anthocyanin in all tissues, resulting in red poplar plants. One bHLH cofactor, bHLH131 was shown to interact with both MYB activators and repressors and required by MYB activators to activate flavonoid gene promoters. This indicate an important role of bHLH131 in the flavonoid biosynthesis. Proanthocyanidin MYB activators, MYB134 and MYB115 could activate each other. This indicates a positive feedback loop of proanthocyanidin MYB activators. Interestingly, repressor MYB165 suppressed expression of other flavonoid MYB repressors including MYB194 and MYB182, which shows a negative feedback loop of MYB repressors. The expression of bHLH131 was also regulated by MYB activators and repressors. These results reveal the complex interaction between these regulators. iv Unexpectedly, overexpression MYB134, MYB115 or MYB117 poplars upregulated flavonoid 3’5’-hydroxylase and cytochrome b5 genes, and lead to enhanced flavonoid B- ring hydroxylation and an increased proportion of delphinidin, prodelphinidin and myricetin. MYB repressors downregulated flavonoid 3’5’-hydroxylase. Overexpression of flavonoid 3’5’-hydroxylase in poplar confirmed its function in enhancing B-ring hydroxylation. However, overexpression of cytochrome b5 in flavonoid 3’5’-hydroxylase- overexpressing plants did not further increase flavonoid B-ring hydroxylation. Thus its role in flavonoid B-ring hydroxylation remained unclear. These results show that flavonoid MYBs could also alter flavonoid structure. Together, these studies outline the complex regulatory network formed by flavonoid MYB activators and repressors, and bHLH cofactors controlling both flavonoid accumulation and structure. v Table of Contents Supervisory Committee .................................................................................................. ii Abstract ......................................................................................................................... iii Table of Contents............................................................................................................ v List of Tables ................................................................................................................. ix List of Figures ................................................................................................................ x Acknowledgments ....................................................................................................... xiii List of Abbreviations ................................................................................................... xiv Chapter 1 : General introduction ..................................................................................... 1 1.1 Flavonoid biosynthesis, structures and functions ................................................... 1 1.2 Poplar as a model woody plant for the study of phenylpropanoid biosynthesis. ..... 4 1.3 Dissertation content and structure .......................................................................... 4 Chapter 2 : Complex regulation of proanthocyanidin biosynthesis in plants by R2R3 MYB activators and repressors ....................................................................................... 7 This chapter will be published as a chapter in Recent Advances in Polyphenol Research, Vol 7 (Ma and Constabel, 2020). ................................................................. 7 2.1 Introduction to PAs and flavan-3-ols ..................................................................... 7 2.2 Regulation of PA and flavonoid biosynthesis by MYB transcription factors .......... 9 2.3 The importance of repressor MYBs in PA and flavonoid metabolism .................. 12 2.4 The complex interactions of PA MYB activators, MYB repressors and bHLH transcription factors .................................................................................................. 13 2.5 Developmental and plant hormone mediated regulation of the PA pathway via MYBs ....................................................................................................................... 16 2.6 Stress activation of PA synthesis by MYBs in poplar and other woody plants ..... 17 2.7 Summary and Conclusions .................................................................................. 19 Chapter 3 : The poplar MYB115 and MYB134 transcription factors regulate proanthocyanidin synthesis and structure ...................................................................... 20 3.1 Abstract .............................................................................................................. 20 3.2 Introduction ........................................................................................................ 20 3.3 Results ................................................................................................................ 25 3.3.1 Microarray analysis of MYB134-overexpressing transgenic poplar identifies new poplar MYB PA regulators ............................................................................ 25 3.3.2 Transgenic plants overexpressing MYB115 show enhanced accumulation of PA ........................................................................................................................ 28 3.3.3 Analysis of gene expression in MYB115 overexpressors and comparison to MYB134 overexpression ....................................................................................... 28 3.3.4 MYB115 and MYB134 interact with bHLH131 and activate multiple flavonoid promoters in transiently transformed poplar cells ................................... 32 vi ............................................................................................................................. 35 3.3.5 MYB115-overexpression leads to reduced concentrations of salicinoid phenolic glycosides and enhanced flavonoid B-ring hydroxylation ........................ 36 3.4 Discussion ........................................................................................................... 41 3.4.1 The poplar MYB115 gene encodes a new MYBPA1-type regulator active in leaves .................................................................................................................... 41 3.4.2 MYB115 and MYB134 are components of a gene regulatory network for PA synthesis ............................................................................................................... 42 3.4.3 MYB134 and MYB115 overexpression leads to reduced accumulation of phenolic glycosides and a greater extent
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