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Shanjida Khan Functional characterization of DUF642 genes in Arabidopsis thaliana by Shanjida Khan A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Plant Biology Department of Biological Sciences University of Alberta © Shanjida Khan, 2015 ABSTRACT DOMAIN OF UNKNOWN FUNCTION 642, (DUF642), is an uncharacterized protein family in the Pfam database, a large collection of protein families. In Arabidopsis thaliana there are 10 proteins that contain DUF642 domains. DUF642 appears to be specific to plants and is present in gymnosperms, monocots and dicots. The present study was designed to investigate the biochemical function and physiological role of two Arabidopsis DUF642 genes, AT5G25460 (DGR2) and AT5G11420 (DUFB). The three dimensional structures of DGR2 and DUFB proteins were predicted by I-TASSER and validated by Ramachandran plot using RAMPAGE Server. Structural models indicated that DGR2 and DUFB showed similarity to carbohydrate binding proteins with hydrolase and carbon-oxygen lyase activity, respectively. Translation fusions with reporter genes showed a punctate pattern of subcellular localization within the cytoplasm, which did not co-localize with the Sec21 Golgi marker but was immediately adjacent to each other, suggesting DGR2 localizes to the trans-Golgi network. DGR2 and DUFB were expressed heterologously in E. coli but sufficient purified proteins could not be obtained for downstream functional assays. Although both DGR2 and DUFB have high sequence similarity (93.4% nucleotide identity), and were presumed to be paralogs, they were expressed in complementary spatial domains according to expression patterns of reporter genes and qRT-PCR analysis. GUS reporter fusions of DGR2 were expressed in the root apex and the later stages of lateral root primordial (LRP) where cells are dividing and elongating whereas DUFB was expressed in the elongating tissues of roots and not in LRP. Both genes were responsive to auxin identified by reporter gene assay where promoter region sequences of DGR2 and DUFB were fused to the GUS gene. T-DNA insertion mutants (Salk_042864 for DGR2 and Salk_094931 for ii DUFB), RNAi, and DGR2 and DUFB overexpressing plants showed no morphological differences from wild-type phenotypes, therefore, metabolic profiling of these mutant plants was performed by gas chromatography/mass spectrometry to reveal metabotypes. The results suggested that DGR2 and DUFB both affected TCA cycle intermediates and were involved in the carbohydrate metabolism. In addition to DGR2 and DUFB characterization in Arabidopsis, a portion of Ph.D. research work included metabolic profiling of developing flax seeds by GC/MS. In summary, we have generated predicted 3D models of DGR2 and DUFB. Subcellular localization revealed that DGR2 possibly localizes to the trans-Golgi network. We speculated that DGR2 is required for cell elongation and division whereas DUFB is required for cell elongation in Arabidopsis. Metabolite profiling of the Arabidopsis T-DNA insertion mutants, RNAi and overexpression plants of DGR2 and DUFB reveals metabolic phenotypes previously unidentified and illustrate perturbation of TCA cycle. Both proteins may influence growth by modifying probably pectin thereby perturbed primary metabolic processes. Both genes are expressed E. coli but failed to obtain purified proteins. The metabolic profiling of developing flax seeds by GC/MS identified unique metabolites and the pathways perturbation during different stages of flax seed development. iii Dedication This thesis is proudly dedicated To my husband, Sajjad Khandker And To our two children, Samiha Khandker and Sakib Khandker iv ACKNOWLEDGEMENT First and foremost I want to express my heartfelt thanks and gratitude to my supervisor, Dr. Michael Deyholos. It has been an honor to be his Ph.D. student. Throughout my Ph.D. study, he has been actively interested in my research work and has always been provided patience guidance encouragement and outstanding advices. His enthusiasm and passion for his research was contagious and motivational for me. I greatly appreciate all his contributions of time, ideas, and funding which enable me to peruse my Ph.D. successfully. I would also like to thank my committee members, Dr. Shelagh Campbell and Dr. Enrico Scarpella, for their valuable advices and encouragement. I would like to thank Dr. Enrico Scarpella who helped me and trained me on focal microscopy which enabled me to perform the subcellular localization and co-localization studies discussed in this dissertation. I would like to thank Dr. Ramanarayan Krishnamurthy who trained me how to perform metabolic profiling using GC/MS and provided suggestion during the metabolic profiling studies in my Ph.D. work. I also like to thank Erik Bergen who helped me to set up GC/MS apparatus. I would like to thank Dr. Muhammad Rahman for his suggestion and help during the heterologous protein expression and purification experiment. I would like to thank all past and present members of Dr. Deyholos lab (Mary De Pauw, Dr. Neil Hobson, Dr. David Pinzon, and Dr. Joshua McDill, Haiyan Zhuang, Kashfia Faruque Zhu Dan, Ningyu Zhang, Anupreeti Ramdoss, Dr. Abdur Rashid, Dr. Manjeet Kumari, Leonardo Galindo, Dr. Rowshon) for their immense contribution to my professional time and good advices during my stay in this lab. Finally, I would like to thank my family for all their support and encouragement during the tough times in the Ph.D. pursuit. v Table of Contents 1. Chapter 1………………………………………………………………………………………1 1.1. Literature review………………………………………………………………….1 1.1.1. Domains of unknown function (DUFs)…………………………………….2 1.1.2. Domain of unknown function 642 (DUF642)……………………………...3 1.1.3. Plant cell wall……………………………………………………………….5 1.1.4. Plant cell wall polysaccharides……………………………………………..6 1.1.4.1. Cellulose………………………………………………………………….6 1.1.4.2. Hemicellulose…………………………………………………………….6 1.1.4.3. Xyloglucan………………………………………………………………..6 1.1.4.4. Mannan…………………………………………………………………...7 1.1.4.5. Xylan……………………………………………………………………..7 1.1.4.6. Pectin……………………………………………….…………………….8 1.1.4.7. Homogalacturonan……………………….………………………………8 1.1.4.8. Rhamnogalacturonan I……………………………………………………8 1.1.4.9. Rhamnogalacturonan II…………………………………………………..9 1.1.5. Matrix cell wall polysaccharides biosynthesis in the Golgi ………….……9 1.1.6. Plant growth and development……………………………………………10 1.1.7. Approaches to characterize the function of an unknown gene……………11 1.1.7.1. Homology search approach……………………………………………..11 1.1.7.1. Reporter genes approach………………………………………………..12 1.1.8. Heterologous protein expression………………………………………….13 1.1.9. Metabolic profiling approach…………………….……………………….13 1.2. Conclusions and objectives…………………………………………………………15 2. Chapter 2……………………………………………………………………………………..17 2.1. In Silico Studies of DUF642 Proteins in Arabidopsis………………………………17 2.2. Introduction……………………………….…………………………………………17 2.3. Materials and Methods………………………………………………………………18 2.3.1. Promoter analysis…………………………………………………………18 2.3.2. Protein structure prediction……………………………………………….18 vi 2.3.3. Structure based function prediction……………………………………….19 2.3.4. Evaluation of Predicted Structures……………………………….……….19 2.3.5. Phylogenetic tree……………………………………………………….…20 2.3.6. Determination of signal peptide, domain assignment and topology predictions………………………………………………………………………..20 2.3.7. Tissue specific expression prediction………………………………….….20 2.4. Results and Discussion……………………………………………………………...20 2.4.1. Tissue specific expression prediction……………………………………..22 2.2.2. Promoter analysis…………………………………………………………25 2.2.3. Protein structure prediction and function analysis………………………..28 2.2.4. Evaluation of predicted structures………………………………………...31 2.2.5. Structure-based function prediction……………………………………….31 2.2.6. Phylogenetic analysis……………………………………………………...37 2.2.7. Subcellular localization prediction………………………………………..39 2.2.8. Predictions of glycosylation……………………………………………….40 2.2.9. Gene co-expression and network analysis………………………...………42 2.3. Conclusions………………………………………………………………………….46 3. Chapter 3……………………………………………………………………………………..47 3.1. Spatial and temporal expression of Two DUF642 Domain-Containing Genes in Arabidopsis……………………………………………………………………………....47 3.2. Introduction…………………………………………………………………….……47 3.3. Materials and methods………………………………………………………………48 3.3.1. Plant materials and growth conditions……………………………….……48 3.3.2. Plasmid construction and plant transformation……………………………49 3.3.3. GUS histochemistry……………………………………………………….49 3.3.4. qRT-PCR analyses……………………………………………………...…50 3.3.5. DGR2 and DUFB expressions in seeds, during germination and growth...50 3.3.6. Hormone treatments………………………………………………………50 3.3.7. Sugar treatments……………………………………….……….…………51 3.3.8. Statistical analysis and graphics……………………..……………………51 3.4. Results………………………………………………………………………………51 vii 3.4.1. Reporter gene assays……………………………………………………..52 3.4.2. Reporter gene expression in seedlings……………………………………52 3.4.3. Reporter gene expression in flowers………………………………………53 3.4.5. Reporter gene expression in response to exogenous hormone……………53 3.4.6. Reporter gene expression in response to monosaccharides………….……54 3.4.7. Quantitative RT-PCR analysis of seedling expression ………………...…54 3.4.8. Hormone and sugar responses of DGR2 and DUFB transcripts…………..55 3.5. Discussion…………………………………………………….………..……56 3.5.1. Spatial expression of DGR2 and DUFB……………………..……………56 3.5.2. Hormonal regulation of DGR2 and DUFB………………….…………….57 3.5.3. Regulation of DGR2 and DUFB by metabolites………………………….59 3.6. Conclusions…………………………………………………………….……………59
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