Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

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dc.contributor.authorYang, Zhenzhenen
dc.contributor.authorZhang, Yetingen
dc.contributor.authorWafula, Eric K.en
dc.contributor.authorHonaas, Loren A.en
dc.contributor.authorRalph, Paula E.en
dc.contributor.authorJones, Samen
dc.contributor.authorClarke, Christopher R.en
dc.contributor.authorLiu, Simingen
dc.contributor.authorSu, Chunen
dc.contributor.authorZhang, Huitingen
dc.contributor.authorAltman, Naomi S.en
dc.contributor.authorSchuster, Stephan C.en
dc.contributor.authorTimko, Michael P.en
dc.contributor.authorYoder, John I.en
dc.contributor.authorWestwood, James H.en
dc.contributor.authordePamphilis, Claude W.en
dc.contributor.departmentSchool of Plant and Environmental Sciencesen
dc.date.accessioned2020-04-20T13:13:05Zen
dc.date.available2020-04-20T13:13:05Zen
dc.date.issued2016-11-08en
dc.description.abstractHorizontal gene transfer (HGT) is the transfer of genetic material across species boundaries and has been a driving force in prokaryotic evolution. HGT involving eukaryotes appears to bemuch less frequent, and the functional implications of HGT in eukaryotes are poorly understood. We test the hypothesis that parasitic plants, because of their intimate feeding contacts with host plant tissues, are especially prone to horizontal gene acquisition. We sought evidence of HGTs in transcriptomes of three parasitic members of Orobanchaceae, a plant family containing species spanning the full spectrum of parasitic capabilities, plus the free-living Lindenbergia. Following initial phylogenetic detection and an extensive validation procedure, 52 high-confidence horizontal transfer events were detected, often from lineages of known host plants and with an increasing number of HGT events in species with the greatest parasitic dependence. Analyses of intron sequences in putative donor and recipient lineages provide evidence for integration of genomic fragments far more often than retro-processed RNA sequences. Purifying selection predominates in functionally transferred sequences, with a small fraction of adaptively evolving sites. HGT-acquired genes are preferentially expressed in the haustorium-the organ of parasitic plants-and are strongly biased in predicted gene functions, suggesting that expression products of horizontally acquired genes are contributing to the unique adaptive feeding structure of parasitic plants.en
dc.description.adminPublic domain – authored by a U.S. government employeeen
dc.description.notesWe thank Dr. Craig Praul and the Huck Genomics Core Facility for transcriptome sequencing and the gift of Striga genome sequences generated on a trial run of the Illumina HiSeq2500 sequencer that was purchased as NSF Equipment Grant MRI-1229046 (to C.W.d.); Tony Omeis for growing M. californica (with Grindelia host) in the Biology Greenhouse at Penn State University from material originally provided by Alison Colwell; K. Shirasu and S. Yoshida for access to the S. asiatica genome sequence and annotation; D. E. Soltis, M. K. Deyholos, M. W. Chase, and C. Wang for collecting nine of the 10 1KP samples used for HGT validation in this study; Ning Jiang (Michigan State University) for discussion of Pong-like TEs; and J. Naumann, J. Der, J. Palmer, M. Axtell, D. Cosgrove, S. Maximova, and M. Guiltinan for helpful suggestions. This research was supported by NSF Plant Genome Research Program Awards DBI-0701748 and IOS-1238057 (to J.H.W., C.W.d., M.P.T., and J.I.Y.), with additional support from the Plant Biology graduate program (Z.Y., L.A.H., S.J., and H.Z.) and from the Genetics graduate program as well as the Biology Department (Y.Z.) at Penn State University; National Institute of Food and Agriculture Project 131997 (to J.H.W.); and NSF Grant IOS-1213059 (to M.P.T.).en
dc.description.sponsorshipNSF Equipment GrantNational Science Foundation (NSF) [MRI-1229046]; NSF Plant Genome Research ProgramNational Science Foundation (NSF)NSF - Office of the Director (OD) [DBI-0701748, IOS-1238057]; Plant Biology graduate program; Genetics graduate program; Biology Department at Penn State University; National Institute of Food and Agriculture Project [131997]; NSF GrantNational Science Foundation (NSF) [IOS-1213059]en
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1073/pnas.1608765113en
dc.identifier.issn0027-8424en
dc.identifier.issue45en
dc.identifier.pmid27791104en
dc.identifier.urihttp://hdl.handle.net/10919/97834en
dc.identifier.volume113en
dc.language.isoenen
dc.rightsCC0 1.0 Universalen
dc.rights.urihttp://creativecommons.org/publicdomain/zero/1.0/en
dc.subjectHGTen
dc.subjectphylogenomicsen
dc.subjectvalidation pipelineen
dc.subjectgenomic transferen
dc.subjectparasitismen
dc.titleHorizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptationen
dc.title.serialProceedings of the National Academy of Sciences of the United States of Americaen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.dcmitypeStillImageen

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