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ABSTRACT ZHANG, WENHENG. Molecular Evolution of Floral ABSTRACT ZHANG, WENHENG. Molecular evolution of floral homeotic B-class genes in the dogwood genus Cornus (Cornaceae) – gene duplication, selection, and coevolution. (Under the direction of Dr. Qiu-Yun Jenny Xiang). Comparative study of floral homeotic gene evolution through reconstructing gene genealogy is recognized as an important step toward understanding the molecular genetic basis of morphological evolution. The floral homeotic B-class genes, APETALA3 (AP3) and PISTILLATA (PI) encode MADS domain-containing transcription factors required to specify petal and stamen identities in Arabidopsis. My dissertation study investigates AP3- and PI- like gene evolution through genomic DNA in the dogwood genus Cornus (Cornaceae). Our studies show that ancient gene duplications occurred in CorPI genes but were lacking in the CorAP3 gene lineage during diversification of Cornus. Reconstruction of the PI genealogy in Cornus based on partial genomic DNA sequences reveals a dynamic history of gene duplication and loss at different phylogenetic levels. Ancient duplication events produced two ancient paralogs, named CorPI-A and CorPI-B, followed by the subsequent loss of gene copies in different subgroups during the early radiation of the genus. The AP3 genealogy of Cornus found no ancient gene duplication during diversification of the genus, while two divergent gene copies are found in Davidia, a close relative of Cornus. Multiple sequence types are observed for both CorPI and CorAP3 genes within the species of Cornus, suggesting that frequent, independent, and recent gene duplications occurred within species. Functional constraints of B-class genes in Cornus are generally relaxed compared to those observed in other plant groups. More relaxed functional constraints are found in CorPI than in CorAP3, and in AP3- than in PI-like genes in the outgroup genera Alangium and Davidia. Difference in the strength of selection on these paralog loci may be related to maintenance of ancient paralog gene copies in the CorPI gene lineage in Cornus, and also in the AP3-like gene lineage in Davidia. The four positively selected amino acid sites detected on the CorPI genes indicate that the relaxation of functional constraints in CorPI may be due to diversifying or positive selection. Moreover, positive selection acting on these sites may be related to gene duplication. For the CorAP3 loci, however, the relaxed functional constraint may be due to neutral evolution. I also discuss the divergence patterns of these two nuclear genes in Cornus and their potential use as phylogenetic markers. Molecular evolution of floral homeotic B-class genes in the dogwood genus Cornus (Cornaceae) – gene duplication, selection, and coevolution by Wenheng Zhang A dissertation submitted to the Graduate Faculty of North Carolina State University In partial fulfillment of the requirements for the degree of Doctor of Philosophy Botany Raleigh, NC November, 2006 Approved by: Dr. (Jenny) Qiu-Yun Xiang Dr. Michael D. Purugganan Chair of Advisory Committee Co-chair of Advisory Committee Dr. Nina S. Allen Dr. Brian M. Wiegmann DEDICATION To my parents ii BIOGRAPHY Wenheng became interested in plant systematics and later evolutionary biology in her third year of college. She became fascinated with evolution because it encompasses so many disciplines, such as geology, biology, and philosophy. Her master’s thesis, focusing on these interests, was a molecular systematic study of the Dipsacales, a major lineage in the Asterids, the largest group of flowering plants, under the direction of Dr. Zhiduan Chen. The work was published in Molecular Phylogenetics and Evolution. After receiving her master’s degree, Wenheng joined Dr. Jenny Xiang’s plant systematics lab in 2002. Wenheng’s studies have encompassed broad evolutionary topics, such as species level phylogeny of Cornus, comparison of the rates of speciation and molecular evolution in plants of eastern Asia and eastern North America, and biogeographical analysis and molecular dating of cornelian cherries. As a co-author, she published three papers based on these studies. Her dissertation topic is a study of the molecular evolution of the floral homeotic B-class gene in Cornus. Wenheng also enjoys teaching. As a teaching assistant in the Biotechnology program at NCSU, she won the 2006 University Outstanding Teaching Assistant Award. Born in Beijing, China, Wenheng earned her bachelor’s degree in pharmacy, with honors, from Beijing Medical University in 1998 and her master’s degree from Beijing University in 2001. Wenheng's long-term goal is to teach, continue her research and to work closely with students and colleagues to find answers to questions on plant systematics, molecular evolution, and evolutionary developmental biology. She married Jun He in 2002. Jun is now a graduate student in the Department of Bioinformatics and Computational Biology at George Mason University. iii ACKNOWLEDGMENTS My deepest gratitude goes to my advisor, Dr. Jenny Xiang, for her insight, guidance, enthusiasm, support, and patience. Although Jenny became sick before my defense, she continued to help with my dissertation revision. I am grateful to my committee members, Dr. Michael D. Purugganan, Dr. Brian M. Wiegmann, and Dr. Nina S. Allen for their insightful comments on my research and for their encouragement. I especially want to thank Dr. Brian M. Wiegmann who extended considerable effort toward improving the English in my dissertation. Many thanks also go to the current and former members of the Xiang Lab, David Thomas, Chuanzhu Fan, Kemei Ding, Jennifer Modliszewski, Melinda Peters, Alexandra Krings, Kathy McKeown, Chunmiao Feng, and AJ Harris for their friendship and for sharing their expertise. I particularly want to thank the following people who gave me help with experiments and data analyses: David Thomas for assistance with sequencing; Kemei Ding for help with collecting some of the AP3 data, and Jun He for helping with histogram analysis and generating figures using the Excel program. I thank Dr. Jer-Ming Hu and Michael Frolich who provided primers and mRNA sequence data of Cornus florida and Cornus alba for this study. My special thank you goes to Dr. David E. Boufford for helpful discussions and for kindly proofreading the dissertation. I also want to thank the Deep Time Program, the Department of Botany and University Graduate Student Association for travel support during my study. This study was supported in part by National Science Foundation grants to Q-Y (J.) Xiang (NSF-DEB 0129069 and DEB 0444125). iv TABLE OF CONTENTS List of Tables………………………………………………………………………………...vii List of Figures……………………………………………………………………….………...x List of Abbreviations………………………………………………………………………..xiii Chapter I. Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae)…….…………………………………………………………...…………………1 Abstract…………………………………………….…………………………..……2 Introduction………………………………………….………………………………3 Materials and Methods……………………….…………………………………...…9 Results…………………………………...…………………………………………19 Discussion……………………………….………………..………………….…….30 Conclusion……………………………....………………..………………….…….39 Future directions…………………........…………………..…………….….…..….39 Acknowledgement………………….………………………..……………….……40 References…………………………….……………………..………………..……40 Tables…………………………….…………………………..…………….………57 Figures………………………….…………………………..………………………70 Chapter II. Molecular evolution of APETALA3-like genes in the dogwood genus Cornus (Cornaceae)…….………………………………………...………..…………………………92 Abstract………………………………………….………..…………………..……93 Introduction……………………………………….……..…………………………94 Materials and Methods…………………….…………..………………………...…97 v Results………………………………….…………………………………………105 Discussion……………………………….………………………………….…….112 Acknowledgement………………….……………………………………….……115 References…………………………….……………………………………..……116 Tables…………………………….……………………………………….………125 Figures………………………….…………………………………………………134 Chapter III. Comparison of evolutionary patterns of two floral homeotic B-class genes PISTILLATA and APETALA3 in the dogwood genus Cornus (Cornaceae)........……...……148 Abstract………………………………………….…………………………..……149 Introduction……………………………………….………………………………150 Materials and Methods…………………….…………………………………...…154 Results………………………………….…………………………………………157 Discussion……………………………….………………………………….…….163 Acknowledgement………………….……………………………………….……172 References…………………………….……………………………………..……173 Tables…………………………….……………………………………….………182 Figures………………………….…………………………………………………189 vi LIST OF TABLES I. Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae) Table 1. Source of plant materials used in this study and information of clones analyzed….……….…….…….…….…….…….…….….….…….…….…….………......…57 Table 2. Various analyses which allow different dN/dS ratios among CorPI-A, CorPI-B and outgroups to detect differences of selection forces (ω = dN/dS) between CorPI of Cornus and PI-like genes in outgroups using PAML 3.15..……………..……………..…59 Table 3. Results of Likelihood Ratio Tests (LRTs) for significance in differential selection force (ω = dN/dS) between CorPI of Cornus and PI-like genes in the outgroup genera Alangium and Davidia...……….……….…….……….…….……….……….………60 Table 4. Parameters estimated for the PISTILLATA-like genes in Cornus based on various codon-based substitution models implemented in PAML 3.15 to test selection....…61 Table 5. Comparisons of models (from Table 4) applied to the Likelihood Ratio Tests (LRTs) for testing heterogeneous selection at amino acid sites in CorPI genes........…62 Table 6. Amino acid variation
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