Horizontal Acquisition of Multiple Mitochondrial Genes from a Parasitic Plant Followed by Gene Conversion with Host Mitochondrial Genes
Total Page：16
File Type：pdf, Size：1020Kb
University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Center for Plant Science Innovation Plant Science Innovation, Center for 2010 Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes Jeffrey P. Mower University of Nebraska-Lincoln, [email protected] Saša Stefanović University of Toronto Weilong Hao University of Toronto, Toronto Julie S. Gummow University of Nebraska-Lincoln Kanika Jain University of Nebraska-Lincoln See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/plantscifacpub Part of the Plant Sciences Commons Mower, Jeffrey P.; Stefanović, Saša; Hao, Weilong; Gummow, Julie S.; Jain, Kanika; Ahmed, Dana; and Palmer, Jeffrey D., "Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes" (2010). Faculty Publications from the Center for Plant Science Innovation. 52. https://digitalcommons.unl.edu/plantscifacpub/52 This Article is brought to you for free and open access by the Plant Science Innovation, Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Center for Plant Science Innovation by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Jeffrey P. Mower, Saša Stefanović, Weilong Hao, Julie S. Gummow, Kanika Jain, Dana Ahmed, and Jeffrey D. Palmer This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ plantscifacpub/52 Mower et al. BMC Biology 2010, 8:150 http://www.biomedcentral.com/1741-7007/8/150 RESEARCH ARTICLE Open Access Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes Jeffrey P Mower1,2*,Saša Stefanović1,3, Weilong Hao1,4, Julie S Gummow1, Kanika Jain2, Dana Ahmed2, Jeffrey D Palmer1 Abstract Background: Horizontal gene transfer (HGT) is relatively common in plant mitochondrial genomes but the mechanisms, extent and consequences of transfer remain largely unknown. Previous results indicate that parasitic plants are often involved as either transfer donors or recipients, suggesting that direct contact between parasite and host facilitates genetic transfer among plants. Results: In order to uncover the mechanistic details of plant-to-plant HGT, the extent and evolutionary fate of transfer was investigated between two groups: the parasitic genus Cuscuta and a small clade of Plantago species. A broad polymerase chain reaction (PCR) survey of mitochondrial genes revealed that at least three genes (atp1, atp6 and matR) were recently transferred from Cuscuta to Plantago. Quantitative PCR assays show that these three genes have a mitochondrial location in the one species line of Plantago examined. Patterns of sequence evolution suggest that these foreign genes degraded into pseudogenes shortly after transfer and reverse transcription (RT)- PCR analyses demonstrate that none are detectably transcribed. Three cases of gene conversion were detected between native and foreign copies of the atp1 gene. The identical phylogenetic distribution of the three foreign genes within Plantago and the retention of cytidines at ancestral positions of RNA editing indicate that these genes were probably acquired via a single, DNA-mediated transfer event. However, samplings of multiple individuals from two of the three species in the recipient Plantago clade revealed complex and perplexing phylogenetic discrepancies and patterns of sequence divergence for all three of the foreign genes. Conclusions: This study reports the best evidence to date that multiple mitochondrial genes can be transferred via a single HGT event and that transfer occurred via a strictly DNA-level intermediate. The discovery of gene conversion between co-resident foreign and native mitochondrial copies suggests that transferred genes may be evolutionarily important in generating mitochondrial genetic diversity. Finally, the complex relationships within each lineage of transferred genes imply a surprisingly complicated history of these genes in Plantago subsequent to their acquisition via HGT and this history probably involves some combination of additional transfers (including intracellular transfer), gene duplication, differential loss and mutation-rate variation. Unravelling this history will probably require sequencing multiple mitochondrial and nuclear genomes from Plantago. See Commentary: http://www.biomedcentral.com/1741-7007/8/147. Background it occurs through such well-studied processes as trans- Horizontal gene transfer (HGT) is the transmission of formation, conjugation and transduction [1,2]. HGT is genes across species boundaries and/or mating barriers. also relatively common and evolutionarily important in HGT plays a major role in prokaryotic evolution, where certain phagotrophic protists [3-6], with food prey often serving as the source of these transferred genes [7]. * Correspondence: [email protected] However, relatively few cases of HGT have been 1 Department of Biology, Indiana University Bloomington, Bloomington, reported in most multicellular, non-phagotrophic Indiana 47403, USA Full list of author information is available at the end of the article © 2010 Mower et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Mower et al. BMC Biology 2010, 8:150 Page 2 of 16 http://www.biomedcentral.com/1741-7007/8/150 eukaryotes and little is known about the mechanisms of intermediate [34,35] or directly via DNA [36-38]. There- transfer [8]. fore, either or both routes may also be available for HGT. For the most part, HGT in plants is comparable to Another largely unanswered question is whether the that of other multicellular eukaryotes - it is a rare nucleic acid is nakedly transferred or packaged inside a phenomenon. Despite intense investigations of geneti- vector. Double-stranded genomic DNA is known to per- cally modified crops, due to the potential for transgene sist for thousands of years in specific environmental escape, there are very few examples of plants donating conditions [39,40], whereas single-stranded RNA or com- genes to any non-plant species [9]. Other than the mas- plementary DNA (cDNA) is not expected to fare as well. sive migration of bacterial genes into the nucleus after Potential vectors for a packaged transfer include viruses, the endosymbiotic establishment of the mitochondrion bacteria, fungi, insects and mitochondria themselves. and plastid [10-12], the transfer of non-plant genes into This last route is supported by two observations: transfer plants is also uncommon. Perhaps the best examples may occur by direct contact between donor and recipient come from the transfer of infectious plasmids from plants; and plant mitochondria (but not plastids) are well Agrobacterium [13,14], the transfer of a mobile group I known to fuse [41,42], accompanied by intergenomic intron from a fungus [15,16] and the ancient transfer of recombination in somatic hybrids [43,44]. Finally, which a few fungal genes into angiosperm nuclear genomes of the three plant genomes is the site of integration of [17]. Horizontal transmission between plants, at the foreign plant mitochondrial genes is largely unexplored. nuclear level, has so far been documented for only a few Although some analyses have provided evidence for transposable elements and genes [18-21]. At the plastid mitochondrial integration [23,25,30,31], the possibility level, plant-to-plant HGT is apparently non-existent or that foreign sequences of mitochondrial origin reside, at least exceedingly rare. No cases were discovered after instead, in the nucleus has been raised [45,46] because the examination of 42 complete plastid genomes from nuclear (but not plastid) genomes readily incorporate representative green plants and red algae plus a single sequences of mitochondrial origin, at least via intracellu- glaucophyte [22] and no reports have emerged from the lar gene transfer [36-38]. many subsequently-sequenced plastid genomes. We previously reported on two independent cases of Although plastid and nuclear gene transfer appears to be horizontal transfer of the mitochondrial atp1 gene from rare among plants, a significant body of evidence indicates different parasitic plant groups into genus Plantago [27]. that plant-to-plant transfer of mitochondrial genes occurs In one case, we identified the donor group as the parasi- with surprising frequency (for examples see [23-31]). In tic genus Cuscuta (dodders; Convolvulaceae) and the most cases, the mechanisms of mitochondrial transfer recipient as the common ancestor of a small clade of remain speculative, with possibilities including: direct con- three closely-related Plantago species, Plantago corono- tact between donor and recipient plants; uptake of DNA pus, P. macrorhiza and P. subspathulata (out of 43 spe- from the environment; and transfer of DNA via vectors cies sampled). As this transfer event was recent, and the such as viruses, bacteria or fungi [23-25]. However, various donor and recipient lineages are well-defined, it is an lines of evidence suggest that mitochondrial