C4 Photosynthetic Evolution
Total Page：16
File Type：pdf, Size：1020Kb
C4 PHOTOSYNTHETIC EVOLUTION: SUB-TYPES, DIVERSITY, AND FUNCTION WITHIN THE GRASS TRIBE PANICEAE _______________________________________ A Dissertation presented to the Faculty of the Graduate School at the University of Missouri-Columbia _______________________________________________________ In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy _____________________________________________________ by JACOB DANIEL WASHBURN Dr. J. Chris Pires, Dissertation Supervisor MAY 2017 The undersigned, appointed by the dean of the Graduate School, have examined the dissertation entitled: C4 PHOTOSYNTHETIC EVOLUTION: SUB-TYPES, DIVERSITY, AND FUNCTION WITHIN THE GRASS TRIBE PANICEAE Presented by Jacob Daniel Washburn, a candidate for the degree of doctor of philosophy, and hereby certify that, in their opinion, it is worthy of acceptance. _____________________________ Dr. J. Chris Pires _____________________________ Dr. James A. Birchler _____________________________ Dr. Paula McSteen _____________________________ Dr. Gavin Conant ACKNOWLEDGEMENTS I would first like to thank my beautiful wife and sweetheart Melinda for her constant companionship, support, and sacrifice over the past five years. Also my three children: Nathan, Sam, and Emma. The four of you have been, and continue to be my inspiration, and my happiness. I also want to thank my parents, Shelley and Kevin Washburn, who instilled in me a love for learning and for hard work. This degree is for you as well. I also thank my advisor Chris for being the most supportive, helpful, and forward- thinking mentor I have ever had the privilege of associating with. I credit you with the success I have had in grant writing during my Ph.D., and with many of the life skills I have learned. My co-advisor Jim has also been an incredible help. Jim, in my mind you are the epitome of a scientist. I also want to thank Gavin for serving on my committee, and for mentoring me in writing, and in thinking like a scientist. Paula, thank you for mentoring me while we served together on the hiring committee, as well as being a crucial member of my dissertation committee. I also wish to thank the Division of Biological Sciences’ staff, students, and faculty for providing such a stimulating and supportive environment. Lastly, I want to thank my church community for their support, and my Heavenly Father for enabling and assisting me in accomplishing this great task. ii TABLE OF CONTENTS ACKNOWLEDGEMENTS ............................................................................................ II LIST OF ILLUSTRATIONS .......................................................................................... V LIST OF TABLES ....................................................................................................... VIII ABSTRACT ..................................................................................................................... IX CHAPTER 1: CONVERGENT EVOLUTION AND THE ORIGIN OF COMPLEX PHENOTYPES IN THE AGE OF SYSTEMS BIOLOGY .......................................... 1 ABSTRACT ....................................................................................................................... 2 INTRODUCTION ................................................................................................................ 3 APPROACHES FOR ANALYZING CONVERGENT EVOLUTION – PAST AND PRESENT ......... 12 FUTURE PROSPECTS FOR INVESTIGATING CONVERGENT EVOLUTION ............................ 21 CONCLUSIONS ................................................................................................................ 31 LITERATURE CITED ........................................................................................................ 33 CHAPTER 2: PHYLOGENY AND PHOTOSYNTHESIS OF THE GRASS TRIBE PANICEAE ...................................................................................................................... 63 ABSTRACT ..................................................................................................................... 64 INTRODUCTION .............................................................................................................. 65 MATERIALS AND METHODS ............................................................................................ 69 RESULTS ........................................................................................................................ 74 DISCUSSION ................................................................................................................... 76 ACKNOWLEDGMENTS .................................................................................................... 83 LITERATURE CITED ........................................................................................................ 85 CHAPTER 3: GENOME-GUIDED PHYLO-TRANSCRIPTOMICS: IMPROVING THE QUALITY OF INFERRED ORTHOLOGS ..................................................... 103 ABSTRACT ................................................................................................................... 104 MATERIALS AND METHODS ......................................................................................... 111 RESULTS ...................................................................................................................... 115 DISCUSSION ................................................................................................................. 121 FUNDING ...................................................................................................................... 125 ACKNOWLEDGMENTS .................................................................................................. 125 REFERENCES ................................................................................................................ 126 CHAPTER 4: THE SUB-TYPES OF C4 PHOTOSYNTHESIS: A TRANSCRIPTOMIC AND EVOLUTIONARY APPROACH TO UNDERSTANDING THEM IN THE GRASSES. ..................................................... 147 ABSTRACT ................................................................................................................... 148 INTRODUCTION ............................................................................................................ 149 MATERIALS AND METHODS ......................................................................................... 152 RESULTS AND DISCUSSION ........................................................................................... 155 CONCLUSIONS .............................................................................................................. 162 REFERENCES ................................................................................................................ 165 CHAPTER 5: FUTURE DIRECTIONS ..................................................................... 176 INCREASING OUR UNDERSTANDING OF THE PANICEAE PHYLOGENY ............................ 176 iii INCREASING OUR UNDERSTANDING OF C4 SUB-TYPE EVOLUTION, DIVERSITY, AND SUB- TYPE MIXING ............................................................................................................... 178 IMPLICATIONS OF C4 SUB-TYPES FOR CROP IMPROVEMENT ........................................ 179 APPENDIX 1: ODE TO ENERGY ............................................................................. 181 APENDIX 2: C4 PHOTOSYNTHESIS ....................................................................... 182 VITA .............................................................................................................................. 183 iv LIST OF ILLUSTRATIONS Figure 1.1 - Ways of explaining convergent evolution. Line drawings representing the evolutionary histories of distinct theoretical lineages with a convergent phenotype, and how these lineages might be expected to evolve under selection, constraint, or drift. ..... 61 Figure 1.2 - Convergent evolution of C4 photosynthesis in the PACMAD grasses. A phylogenetic tree showing multiple origins of C4 photosynthesis within a subsection of the grasses (family Poaceae) called the PACMAD. Lineages using the C4 photosynthetic type are marked in red while those using the ancestral type (C3) are marked in black. Note that the distribution of C4 lineages shown here are not proportional to those found across angiosperms as a whole and are only an estimate of the number of origins within grasses. Several of these origins may be further subdivided or combined as future research demonstrates better support for distinct clades. The tree is re-drawn from Grass Phylogeny Working Group II, (2012) and Washburn et al., (2015). ................................ 62 Figure 2.1 - Phylogenetic understandings of the tribe Paniceae. Left: Previous phylogeny of the tribe Paniceae redrawn from the Grass Phylogeny Working Group II (2012). Right: New phylogeny from the 78 chloroplast gene data set presented in this study. Branches with a posterior probability of less than 0.8 are collapsed into polytomies on both phylogenies. Figure is drawn using the traditional three C4 sub-type system but can be easily interpreted based on the two sub-type system by replacing PCK with NAD-ME. 92 Figure 2.2 - Chloroplast phylogeny of the tribe Paniceae based on 78 loci. Maximum likelihood (ML) tree with both bootstraps (BS) and Bayesian Posterior Probabilities (PP) marked on the branches. Unmarked branches have values of 100 for both BS and PP. Species are colored by photosynthetic sub-type except for outgroups which have not been colored.