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The Pennsylvania State University the Graduate School The The Pennsylvania State University The Graduate School The Huck Institutes of Life Sciences IDENTIFICATION AND FUNCTIONAL CHARACTERIZATION OF GLYCOSYL HYDROLASE FAMILY 1 (GH1) GENES ACTING ON MONOLIGNOL SUBSTRATES IN POPLAR AND LOBLOLLY PINE A Thesis in Integrative Biosciences by Anushree Sengupta © Anushree Sengupta Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Science August 2012 The thesis of Anushree Sengupta was reviewed and approved* by: John E. Carlson Professor of Molecular Genetics Thesis Adviser Claude dePamphilis Professor of Biology Dawn Luthe Professor of Plant Stress Biology Teh Hui-Kao Professor of Biochemistry & Molecular Biology Chair, Intercollege Graduate Degree Program in Plant Biology *Signatures on file in the Graduate School. ii Abstract ß-glucosidases (BGLUs) are members of the Glycosyl hydrolase family 1 (GH1) group of enzymes that play important roles in several physiological processes in plants. Coniferin ß - glucosidase (CBG) identified by Dharmawardhana et al. (1995) in Pinus contorta was the first BGLU identified to specifically act on monolignol substrates. It removes a glucoside from the glucosylated form of coniferyl alcohol, coniferin, prior to its polymerization into lignin. Our goal is to try to identify the ß-glucosidase genes in poplar and pine that are specific to lignin monomers. We used the pine CBG cDNA sequence as BLAST query against all plant nodes in Phytozome (JGI) to identify other CBG genes and constructed a NJ tree with the sequences obtained manual sequence curation and 1000 bootstrap replicates with the aligned sequences. We retrieved 40 GH1 family genes from the Poplar genome and by phylogenetic analysis identified 6 Poplar genes that cluster with CBG and other lignin monomer specific genes, which includes two forms of the CBG gene in Pinus contorta and four forms of the gene in Pinus taeda identified previously in our lab (Song Liu, unpublished data). We analyzed the expression of the 6 genes identified to be putative lignification genes in the leaves, xylem and phloem samples collected during different time points in Populus balsamifera, a poplar species closely related to P. trichocarpa. Expression analysis of samples of xylem, phloem and leaves collected during April, June and September show a decrease in expression of the genes in from April to September in xylem and iii phloem. The expression is also higher in the vascular tissues where lignin is present than in the leaves. iv Contents LIST OF FIGURES viii LIST OF TABLES x LIST OF ABBREVIATIONS xi LIST OF OVERSIZED MATERIALS (IN ELECTRONIC VERSION) xii ACKNOWLEDGEMENTS xiii CHAPTER 1: INTRODUCTION AND LITERATURE REVIEW 1 Synthesis of monolignols 2 Extracellular steps in lignin biosynthesis 4 Model organisms 7 CHAPTER 2: EVOLUTIONARY ANALYSIS OF THE GLYCOSYL HYDROLASE FAMILY 1 (GH1) GENES IN PLANTS AND IDENTIFICATION OF PUTATIVE GENES INVOLVED IN LIGNIFICATION Introduction 10 Materials and Methods 11 Results 13 Discussion and Conclusions 17 v CHAPTER 3: DETERMINING THE EXPRESSION OF LIGNIN SUB-CLADE GH1 GENES Introduction 32 Materials and Methods Collection of plant tissue samples: 34 qRT-PCR Primer design and validation: 35 Extraction of RNA and qRT-PCR: 36 Normalization of the results 37 Statistical analysis of data 38 Results and Analysis of data Expression of CBG-like genes in Populus balsamifera 40 Expression of CBG-like genes in Pinus taeda 43 Conclusions and Discussion 45 CHAPTER 4: LOCALIZATION OF LIGNIN IN POPLAR STEMS Introduction 59 Materials and Methods: Collection of specimens 59 Preparation for microscopy 60 vi Results 61 Conclusions and Discussion 62 CHAPTER 5: GENERAL DISCUSSION AND THE BROADER PERSPECTIVE 65 LITERATURE CITED 69 APPENDIX A ALL SEQUENCES IN PHYLOGENETIC TREE 75 APPENDIX B TABLES, FIGURES AND RAW DATA FOR CHAPTER 3 PART A – Poplar samples 93 PART B – Loblolly Pine samples 149 vii LIST OF FIGURES Figure1.1 Mode of Action of β-glucosidase 5 Figure 2.1 Available as Supplemental figure 3 in computerized 22 version. NJ analysis of amino acid alignments of the putative lignin clade (PLC) of GH1 family genes that contains CBG-like genes which putatively act on lignin monomer substrates. Figure 2.2 A Maximum-Likelihood tree (ML) of the PLC obtained 23 by amino acid alignments and 500 boot strap reiterations. Available as Supplemental figure 3 in computerized version Figure 2.3 Synteny of putative Lignification b-glucosidase in 24 Populus showing tandem duplicates in Poplar PLC genes Figure 2.4A Muscle v3.8 alignment of the CDS sequence of 25 PoptrGH1-26 and PoptrGH1-27 Figure 2.4B Muscle v3.8 alignment of 100bp upstream region of 27 PoptrGH1-26 and PoptrGH1-27 Figure 2.5A and B Comparison of the 6 Populus CBG-like genes with the 29 29 predicted ancestral GH1 gene structure, consisting of 13 exons Figure 2.6A Sequence Logos for amino acids in the catalytic 30 acid/base domain in all GH1 sequences viii Figure 2.6B Sequence Logos for amino acids in the catalytic 30 acid/base domain in Lignin clade only (PLC) Figure 2.7A Sequence Logos for amino acids in the catalytic 31 nucleophile domain in all GH1 sequences Figure 2.7B Sequence Logos for amino acids in the catalytic 31 nucleophile domain in the Lignin clade only (PLC) Figure 3.1 A to D Graphs of dCt using UBQ Vs time in Poplus balsamifera 53 Figure 3.2 A to D Graphs of dCt using PoptrGH1-34 Vs time in Poplus 55 balsamifera Figure 3.3 A and B Graphs of dCt using Act2 Vs time in Pinus taeda 57 Figure 3.4 A and B Percentage graph of dCt using Act2 Vs time in Pinus 58 taeda Figure 4.1 Autofluorescence CLSM images of cross section of 63 Populus balsamifera stem, with 405nm excitation Figure 4.2 Fluorescent CLSM images of cross sections of Populus 64 balsamifera stems stained in basic fuchsin ix LIST OF TABLES Table 2.1 Poplar accession numbers and the corresponding GH1 21 names Table 3.1a Primer Sequences used for RT-PCR assay of gene 48 expression in Poplar Table 3.1b Primer Sequences used for RT-PCR assay of gene 48 expression in Pine Table 3.2a Summary of ANOVA results for comparisons of 49 biological replicates and tissues; data normalized with UBQ11 Table 3.2b Summary of ANOVA results for comparisons of 50 biological replicates and months; data normalized with UBQ11 Table 3.3a Summary of ANOVA results for comparisons of 51 biological replicates and tissues; data normalized with GH1-34 Table 3.3b Summary of ANOVA results for comparisons of 52 biological replicates and months; data normalized with GH1-34 x LIST OF ABBREVIATIONS GH1 Glycosyl Hydrolase Family 1 CBG Coniferin Beta Glucosidase PLC Putative Lignin Clade Poptr Poplar trichocarpa For complete names of all the abbreviations used in phylogenetic tree, please refer to Appendix A. xi LIST OF OVERSIZED MATERIALS (in electronic version) Supplemental Figure 1 Complete NJ tree Supplemental Figure 2 NJ tree of PLC Supplemental Figure 3 ML tree of PLC All Sequences NJ tree Newick PLC NJ Tree Newick PLC ML Tree 100BS newick All Sequences Protein Alignment NEXUS PLC Protein alignment NEXUS xii ACKNOWLEDGEMENTS First of all, I’d like to thank my adviser, Dr.John Carlson and my committee members, Dr.Dawn Luthe , Dr.Claude dePamphilis and former committee member, Dr.David Braun for their help to do this project. I would like to thank the various centers I received funding from which includes the Huck Institutes of Life Sciences, Intercollegiate degree program in Plant Biology, The Schatz Center for Tree Molecular Genetics in the School of Forest Resources at Pennsylvania State University and the Center for Lignocellulose Structure and Function, an Energy Frontier Research Center funded by the US department of Energy. I would also thank Denis S. DiLoreto, Nicole Zembower, Lena Landherr Sheaffer, Paula E. Ralph, Yuannian Jiao, as well as other Carlson Lab members –Joshua Verbano, Joshua R. Herr, Tyler K. Wagner, Chien-Chih Chen, Charles Addo-Quaye, Teodora Best, and various other members of the Plant Biology community. My special acknowledgement goes to my parents and my husband, all of who patiently put up with me and supported me in every step of this project. They stood strong to give me the strength to finish my defense within a couple of months after my mother passed away. Finally, I would like to thank Dr.Howard Salis for allowing me to finish off the thesis while I was working in his lab, and all Salis lab members who have provided wonderful moral support. xiii Chapter 1: Introduction and Literature Review Lignin is an important component of the plant cell wall. Along with cellulose, lignin forms the backbone for plants to stand erect. The deposition of lignin in the cell wall of photosynthetic land plants is considered to have evolved around 430 million years ago (Boudet, 2000). Apart from providing mechanical support, lignin provides hydrophobicity to water conducting cells (Dixon et al., 2001, Taiz and Zeiger, 2006). Lignin also plays a role in plant defense by providing a hydrophobic wall that counters the action of hydrolytic enzymes released by pathogens (Boudet, 2000, Taiz and Zeigler, 2006), and defends against herbivory by making the tissue difficult to digest by herbivores (Rogers and Campbell, 2004). It has also been postulated that lignins play a role in cell wall extension, but that has not yet been convincingly demonstrated (Boudet, 2000). Zhong et al. (1997) demonstrated that in mutants which lacked lignin in interfascicular fibers of Arabidopsis, known as the interfascicular fiber mutant (ifl), the stems grow long and could not stand as erect as the wild type plants, but rather would lie on the ground. But the usefulness of lignin to plants makes it less acceptable for the food and fodder industry as its presence makes fodder difficult for animals to digest.
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