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Exploring the Evolutionary History of Cultivated Rice

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Exploring the Evolutionary History of Cultivated Rice EXPLORING THE EVOLUTIONARY HISTORY OF CULTIVATED RICE: THE ORIGIN AND EVOLUTION OF FRAGRANCE AND THE GENETIC CONTROL OF BLACK HULL COLORATION A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Michael James Kovach May 2010 © 2010 Michael James Kovach EXPLORING THE EVOLUTIONARY HISTORY OF CULTIVATED RICE: THE ORIGIN AND EVOLUTION OF FRAGRANCE AND THE GENETIC CONTROL OF BLACK HULL COLORATION Michael James Kovach, Ph.D. Cornell University 2010 Cultivated Asian rice traveled a long and complex journey from a low-yielding, weedy grass species to the high-yielding staple crop consumed by billions of people today. This journey, driven by human selection, involved a series of genetic changes that transformed the rice plant in many profound ways. Modern genetics and genomics techniques have made it possible to re-trace the history of rice domestication and evolution. This new knowledge not only renders a clearer picture of the evolutionary paths traveled during rice domestication, but it also provides new insights for plant breeders, who are faced with the challenge of feeding an ever-growing human population. This dissertation examines the current body of knowledge pertaining to rice evolution, and in the process, attempts to improve our understanding of the genetic diversity within Oryza sativa and its wild progenitor, Oryza rufipogon . An in- depth haplotype analysis is presented to reveal the origin and evolution of fragrance in rice, which remains one of the most important grain quality characteristics from the perspective of both the international export industry and indigenous peoples who have treasured this trait for centuries. The evolutionary history of the major allele responsible for fragrance in most modern varieties, badh2.1 , is investigated, as well as the origins of several novel fragrance-causing alleles of BADH2 in unique rice germplasm from across Asia. Also, in an effort to further our understanding of the rice domestication syndrome, a genetic mapping study is presented that identifies the causal mutation responsible for a fundamental change during rice domestication: the loss of black pigmentation from the outer covering (hull) of the rice seed. A striking genetic phenomenon is revealed, in which the black hull trait is found to be controlled by an epistatic relationship between two physically linked genes. BIOGRAPHICAL SKETCH Michael was born November 11, 1983 in Baltimore, Maryland to Gerald and Kathleen Kovach. He grew up in Glen Burnie, MD where he attended Point Pleasant Elementary School until the 5 th grade, at which point his family moved to Duncansville, PA. There, Michael attended St. Patrick’s parochial school and then Bishop Guilfoyle High School. Michael was an active member of the cross country team, track and field team, and the ski club. He was also an avid home gardener, and spent his summers working for the Baronner Vegetable Farm in Hollidaysburg, PA, inspiring him to pursue a career in the plant sciences. Michael graduated as valedictorian of his senior class, and was accepted into the Schreyer Honors College at the Pennsylvania State University. While pursuing a Bachelors of Science in Horticulture at Penn State, Michael served as President of the Horticulture Club, completed a life sciences internship at the University of Missouri, conducted a research project on wild tomatoes, and had the opportunity to study briefly in Peru and New Zealand. Michael graduated in 2005 as the College of Agriculture Sciences Class Marshall and entered the PhD program in Plant Breeding & Genetics at Cornell University. Michael’s experiences at Cornell have included attending a workshop at the International Rice Research Institute in the Philippines, studying international agriculture in southern India, presenting his research at a conference in the U.K., and teaching a molecular breeding course at the Biosciences Eastern and Central Africa (BecA) hub in Nairobi, Kenya. Michael is beginning his plant breeding career as a maize Line Development Breeder for Monsanto Co. in Thomasboro, Illinois. iii ACKNOWLEDGMENTS Foremost and above all, I thank God for providing me with life, a loving family, and the vast opportunities and privileges that have made it possible for me to come this far. My awe at the biological complexities of His creation drives my desire to use crop breeding as a means of maximizing life’s potential. My Mom and Dad, who have sacrificed so much to provide me with an excellent education and who have stayed with me through every fault and tribulation, deserve more acknowledgement than could ever be expressed. Without their loving support, I would never have had access to the resources I needed to pursue this degree, nor the self-confidence to always strive to be the best I can be in all that I do. To Susan, who took a chance on me, and proceeded to form me into the thinker, the researcher, the plant breeder, and the person I am today. Also to Rebecca and Steve, for helping me to navigate the bumpy road of a PhD career. I am grateful to the members of the McCouch research program for their valuable critical analysis and helpful comments on my work. I acknowledge financial support from the Plant Genome Program of the National Science Foundation (Award Numbers #0606461 and #0110004), the EU project META-PHOR (FOOD-CT-2006-036220), the College of Agriculture and Life Sciences, and the Department of Plant Breeding and Genetics. iv TABLE OF CONTENTS Biographical Sketch iii Acknowledgements iv Table of Contents v List of Figures vi List of Tables viii Preface ix Chapter 1: Introduction 1 Chapter 2: Leveraging Natural Diversity: Back Through the Bottleneck 11 Chapter 3: New Insights into the History of Rice Domestication 35 Chapter 4: The Origin and Evolution of Fragrance in Rice 70 ................ (Oryza sativa L.) Chapter 5: The Origin of Fragrance in NERICA1 119 Chapter 6: Mapping the Genetic Determinant of Fragrance in 134 ................ Kai Noi Leuang Chapter 7: The Genetic Control of Black Hull in Rice 146 Chapter 8: The Genetic and Geographic Origin of the badh2.1 FNP: 197 ................ Scenarios Chapter 9: Characterization of RC-Mediated Regulation of 207 ................ Proanthocyanidin Biosynthesis as a Prerequisite for a ................ Novel Transgene Containment Strategy in Rice Glossary of Key Terms 245 v LIST OF FIGURES Figure 2.1: The complex domestication process of O. sativa 14 Figure 2.2: Subpopulation structure of O. sativa 15 Figure 2.3: Transgressive segregation 20 Figure 2.4: Rice breeding options: How to generate novelty? 22 Figure 3.1: The domestication transformation— 38 ................. From O. rufipogon to O. sativa Figure 3.2: Subpopulation structure in O. sativa 42 Figure 3.3: The origin and dispersal of cultivated rice 48 Figure 3.4: Haplotype network for the Rc gene 53 Figure 4.1: Subpopulation structure in O. sativa 73 Figure 4.2: Haplotype analysis of the BADH2 gene region 79 Figure 4.3: Extended haplotype homozygosity (EHH) across the 84 ................. BADH2 genomic region Figure 4.4: BADH2 allelic diversity 86 Supplemental Figure 4.1: Extended haplotype homozygosity 111 . .......... (EHH) across the BADH2 genomic region in ...... ..... individual subpopulations Figure 5.1: Results of the badh2.1 allele-specific marker 123 Figure 5.2: The origin of badh2.1 in NERICA1 125 Figure 6.1: Illumina BeadXpress results for 138 ............... .TSN1 x KNL BC 4F2 Figure 6.2: Ex4_F / Ex5_R amplification in KNL 140 Figure 6.3: Genomic DNA and predicted protein of Badh2 141 .................. (wild-type) and badh2.11 (fragrant) alleles Figure 6.4: badh2.11 allele-specific marker 143 vi Figure 7.1: Detailed anatomy of a rice spikelet; Pre-fertilization 147 Figure 7.2: Informative recombinants for hull color from 158 .................. SL population Figure 7.3: Informative recombinants for hull color from 161 .................. Cyb x 506A and Cyb x 549A populations Figure 7.4: Structure of Loc_Os04g38660 and 164 .................. Loc_Os04g38670 with and without 22bp deletion Figure 7.5: Bh-a protein comparisons 165 Figure 7.6: Allele-specific marker for 22 bp deletion 166 Figure 9.1: Model for RC-mediated transcriptional activation of 219 .................. a proanthocyanidin biosynthetic gene in the rice .................. pericarp Figure 9.2: The general proanthocyanidin biosynthetic pathway 222 .................... in plants Figure 9.3: RT-PCR results for proanthocyanidin biosynthetic 224 ................. genes in rice pericarp Figure 9.4: DFR Promoter Deletions 228 Figure 9.5: pCAMBIA1301 and pCAMBIA1301mod 229 Figure 9.6: pCAMBIA1302_mGFP and 230 .................pCAMBIA1302_mGFP5mod vii LIST OF TABLES Table 3.1: Key domestication-related genes cloned in rice 39 Table 4.1: Frequency of badh2.1 allele in wild and cultivated rice 77 Table 4.2: Average nucleotide diversity across BADH2 gene 83 ................. (θπ per kb) Supplemental Table 4.1: Rice accessions used in this study 94 Supplemental Table 4.2: Gene haplotypes for all 242 O. sativa 101 .................. accessions Supplemental Table 4.3: Extended haplotypes for all 242 105 .................. O. sativa accessions and the heterozygous wild .................. accession Supplemental Table 4.4: Novel coding mutations in BADH2 109 Supplemental Table 4.5: Primers used in this study 110 Supplemental Table 5.1: Rice accessions used in this study 126 Supplemental Table 5.2: Primers Used in This
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