Horizontal gene transfer (HGT) is now recognized as a major evolutionary genetic force driving genomic and phenotypic change in the microbial world -- throughout prokaryotes and in many unicellular eukaryotes (all phagotrophic protists). We and others recently discovered the first evidence for widespread HGT within any group of multicellular eukaryotes, finding that horizontal transfer of mitochondrial genes in plants is both frequent and recent. Many of these transfers yield mitochondrial gene duplications (of vertically and horizontally transmitted homologs), whereas others lead to strikingly chimeric genes (part horizontal/part vertical) or repopulate the genome with genes previously transferred to the nucleus. Some of the transferred genes are intact, expressed, and probably functional. One mitochondrial genome has already been identified with multiple, perhaps many horizontally acquired genes. The goal of this study is to build on these exciting findings and conduct the first comprehensive and rigorous study of HGT in multicellular eukaryotes. Because HGT is a fundamental but poorly understood process in genome evolution, these studies will provide an important new perspective on genome structure and function. The maintenance of an intact, functioning genome is critical for human health, and understanding mechanisms of gene exchange is important to the development of gene therapy. This project focuses on plant mitochondrial genomes because their exceptional propensity for HGT and several other attributes make them a model system for investigating HGT in eukaryotes. Studies include targeted macroarray screens of 4000 plants, all-gene sequencing in 200 diverse plants, whole-genome sequencing in 15 plants with exceptionally extensive HGT, and various follow-up studies on specific cases of high interest from the above. Results will address numerous questions concerning rates, patterns, extents, chimeric consequences, donor/recipient relationships, functionality, and mechanisms of HGT across many lineages of plant mitochondrial genomes. Certain of the mechanistic studies follow from emerging evidence suggesting that certain plants and genes are unusually prone to HGT and that a common mechanism of transfer is physical penetration between parasitic plants and their host plants.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM070612-03
Application #
7174292
Study Section
Genetics Study Section (GEN)
Program Officer
Eckstrand, Irene A
Project Start
2005-02-01
Project End
2009-01-31
Budget Start
2007-02-01
Budget End
2008-01-31
Support Year
3
Fiscal Year
2007
Total Cost
$390,174
Indirect Cost
Name
Indiana University Bloomington
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
006046700
City
Bloomington
State
IN
Country
United States
Zip Code
47401
Wu, Zhiqiang; Sloan, Daniel B; Brown, Colin W et al. (2017) Mitochondrial Retroprocessing Promoted Functional Transfers of rpl5 to the Nucleus in Grasses. Mol Biol Evol 34:2340-2354
Richardson, Aaron O; Rice, Danny W; Young, Gregory J et al. (2013) The ""fossilized"" mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biol 11:29
Sloan, Daniel B; Alverson, Andrew J; Chuckalovcak, John P et al. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241
Alverson, Andrew J; Rice, Danny W; Dickinson, Stephanie et al. (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499-513
Alverson, Andrew J; Zhuo, Shi; Rice, Danny W et al. (2011) The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS One 6:e16404
Sanchez-Puerta, Maria V; Abbona, Cinthia C; Zhuo, Shi et al. (2011) Multiple recent horizontal transfers of the cox1 intron in Solanaceae and extended co-conversion of flanking exons. BMC Evol Biol 11:277
Mower, Jeffrey P; Stefanovic, Sasa; Hao, Weilong et al. (2010) Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8:150
Hao, Weilong; Richardson, Aaron O; Zheng, Yihong et al. (2010) Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. Proc Natl Acad Sci U S A 107:21576-81
Alverson, Andrew J; Wei, XiaoXin; Rice, Danny W et al. (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 27:1436-48
Hao, Weilong (2010) OrgConv: detection of gene conversion using consensus sequences and its application in plant mitochondrial and chloroplast homologs. BMC Bioinformatics 11:114

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