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Open Yetingdissertationori.Pdf The Pennsylvania State University The Graduate School Intercollege Graduate Program in Genetics HORIZONTAL GENE TRANSFER STUDIES IN PARASITIC PLANTS OF THE OROBANCHACEAE A Dissertation in Genetics by Yeting Zhang © 2013 Yeting Zhang Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2013 The dissertation of Yeting Zhang was reviewed and approved* by the following: Stephen W. Schaeffer Professor of Biology Chair of Committee Claude W. dePamphilis Professor of Biology Dissertation Advisor Tomas A. Carlo Assistant Professor of Biology John E. Carlson Professor of Molecular Genetics, School of Forest Resources Director of The Schatz Center for Tree Molecular Genetics Naomi Altman Professor of Statistics Robert F. Paulson Professor of Veterinary and Biomedical Sciences Chair, Intercollege Graduate Degree Program in Genetics *Signatures are on file in the Graduate School ii ABSTRACT Parasitic plants, represented by several thousand species of angiosperms, use modified structures known as haustoria to tap into photosynthetic host plants in order to extract nutrients and water. As a result of these direct plant-to-plant connections with their host plants, parasitic plants have unique opportunities for horizontal gene transfer (HGT), the nonsexual transmission of genetic material across species boundaries. There is increasing evidence that parasitic plants have served as the recipients and donors of HGT, but the long-term impacts of eukaryotic HGT in parasitic plants are largely unknown. Three parasitic plant genera from Orobanchaceae (Triphysaria versicolor, Striga hermonthica, and Orobanche aegyptiaca (syn. Phelipanche aegyptiaca)) were chosen for a massive transcriptome-sequencing project known as the Parasitic Plant Genome Project (PPGP). These species were chosen for two reasons. First, the three parasites ranges from facultative hemiparasite to obligate holoparasite, which makes them excellent candidates for understanding the evolution of plants having heterotrophic capacities. Second, because they have destructively impacted important crops, especially Striga hermonthica and Orobanche aegyptiaca (syn. Phelipanche aegyptiaca), they are relatively well studied by scientists working on controlling these harmful parasites. The first half of Chapter 1 is a comprehensive introduction of parasitic plants. The remainder of Chapter 1 is a detailed literature review on HGT studies on plants, particularly parasitic plants. Chapter 2 introduces a gene encoding albumin 1 KNOTTIN-like protein found in Phelipanche aegyptiaca and related parasitic species of family Orobanchaceae that was likely acquired by a Phelipanche ancestor via HGT from a legume host based on phylogenetic analyses. iii Before our research, albumin 1 genes were only known in papilionoid legumes, where they serve dual roles as food storage and insect toxin. The KNOTTINs are well known for their unique “disulfide through disulfide knot” structure and have been extensively studied in various contexts, including drug design. According to genomic sequences from nine related parasite species, 3D protein structure simulation tests, and evolutionary constraint analyses, the parasite gene we identified here retains the intron structure, six highly conserved cysteine residues necessary to form a KNOTTIN protein, and displays levels of purifying selection like those seen in legumes. The albumin 1 xenogene has evolved through more than 150 speciation events over ca. 16 million years, forming a small family of differentially expressed genes that may confer novel functions in the parasites. Moreover, further data show that a distantly related parasitic plant, Cuscuta, obtained two copies of albumin 1 KNOTTIN-like genes from legumes through a separate HGT event, suggesting that legume KNOTTIN structures have been repeatedly co-opted by parasitic plants. Chapter 3 summarizes the HGT findings in the PPGP utilizing a phylogenomic approach in identifying HGT events. Twenty-two published plant genomes (Selaginella moellendorffii, Physcomitrella patens, Amborella trichopoda, Oryza sativa, Brachypodium distachyon, Sorghum bicolor, Phoenix dactylifera, Musa acuminata, Nelumbo nucifera, Aquilegia coerulea, Arabidopsis thaliana, Carica papaya, Fragaria vesca, Glycine max, Medicago truncatula, Populus trichocarpa, Thellungiella parvula, Theobroma cacao, Vitis vinifera, Solanum lycopersicum, Solanum tuberosum, and Mimulus guttatus), two asterid EST datasets (Lactuca sativa and Helianthus annuus), and four PPGP species (Lindenbergia philipensis, Triphysaria versicolor, Striga hermonthica, and Phelipanche aegyptiaca) were used in orthogroup classifications. Phylogenies for each orthogroup were built and customized JAVA scripts were iv used to perform the initial HGT screening. Secondary manual screening was carried out using various criteria. The final findings are presented in this chapter. With each finding, evidence from incongruent phylogenies, expression profiles for HGT genes, potential gene function, evolution constraint analyses, and genomic integration is discussed. The majority of the transgenes show evidence of introns, indicating the HGT transfer happened at the DNA level, and not from a retroprocessed transcript. We also identified two high confidence HGT transgenes in Striga hermonthica located adjacent to each other. This is the first time a genomic integration of length greater than one gene has been identified in a parasitic plant, and suggests that a search for large integration fragments could be fruitful. We are identifying HGT transgenes based on our EST datasets and this may be just the “tip of the iceberg” of HGT in parasitic plants, as a lot of the HGT transgenes in parasitic plant genomes may be highly divergent pseudogenes and may not be expressed. With more genomic data available in the future for the PPGP project, we would be able to tackle this question. We hope that our findings provide a rich pool for functional studies in the parasitic plants’ research community. v TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. ix LIST OF TABLES................................................................................................................... xiv ACKNOWLEDGEMENTS..................................................................................................... xvi Chapter 1 Background of Parasitic Plants .............................................................................. 1 Introduction to Parasitic Plants ........................................................................................ 1 Categories of Parasitic Plants................................................................................... 1 General Introduction of the Haustorium .................................................................. 2 Germination Signals Studies .................................................................................... 3 Studies on Genomes and Evolution of Parasitic Plants............................................ 4 Introduction to Triphysaria versicolor, Striga hermonthica, and Orobanche aegyptiaca ................................................................................................................ 9 Parasitism Degree in Orobanchaceae....................................................................... 9 Evolutionary History and General Information for Orobanchaceae ........................ 10 Ecological Impact of Orobanchaceae....................................................................... 12 Large-Scale Genome Information Studies on Orobanchaceae ................................ 12 Introduction to the Parasitic Plant Genome Project (PPGP)............................................ 14 The Reasons to Initiate the PPGP and its Goals....................................................... 14 The Design and Unique Features of the PPGP ........................................................ 15 The Achievements of the PPGP............................................................................... 17 A Brief Review of Horizontal Gene Transfer in Microorganisms and Plants ................. 19 HGT in Bacteria ....................................................................................................... 19 HGT in Eukaryotes................................................................................................... 21 Chapter 2 Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species [85] ................................................... 33 Background ...................................................................................................................... 33 Results.............................................................................................................................. 36 Identifying the albumin1 gene in Broomrape species.............................................. 36 Genomic sequence features of the albumin 1 gene in Phelipanche aegyptiaca and related species............................................................................................ 38 Incongruent Phylogeny of the albumin1 gene.......................................................... 42 KNOTTIN structure identified in albumin 1 proteins from Phelipanche aegyptiaca ........................................................................................................ 44 Evolution constraint
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