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

Zhenzhen Yang, Yeting Zhang, Eric K. Wafula, Loren A. Honaas, Paula E. Ralph, Sam Jones, Christopher R. Clarke, Siming Liu, Chun Su, Huiting Zhang, Naomi S. Altman, Stephan C. Schuster, Michael P. Timko, John I. Yoder, James H. Westwood, Claude Walker Depamphilis

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Horizontal 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 highconfidence 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.

Original languageEnglish (US)
Pages (from-to)E7010-E7019
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number45
DOIs
StatePublished - Nov 8 2016

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Heterotrophic Processes
Horizontal Gene Transfer
Parasites
Genes
Eukaryota
Orobanchaceae
Plant Structures
Transcriptome
Introns
Sequence Analysis

All Science Journal Classification (ASJC) codes

  • General

Cite this

Yang, Zhenzhen ; Zhang, Yeting ; Wafula, Eric K. ; Honaas, Loren A. ; Ralph, Paula E. ; Jones, Sam ; Clarke, Christopher R. ; Liu, Siming ; Su, Chun ; Zhang, Huiting ; Altman, Naomi S. ; Schuster, Stephan C. ; Timko, Michael P. ; Yoder, John I. ; Westwood, James H. ; Depamphilis, Claude Walker. / Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 45. pp. E7010-E7019.
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abstract = "Horizontal 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 highconfidence 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.",
author = "Zhenzhen Yang and Yeting Zhang and Wafula, {Eric K.} and Honaas, {Loren A.} and Ralph, {Paula E.} and Sam Jones and Clarke, {Christopher R.} and Siming Liu and Chun Su and Huiting Zhang and Altman, {Naomi S.} and Schuster, {Stephan C.} and Timko, {Michael P.} and Yoder, {John I.} and Westwood, {James H.} and Depamphilis, {Claude Walker}",
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Yang, Z, Zhang, Y, Wafula, EK, Honaas, LA, Ralph, PE, Jones, S, Clarke, CR, Liu, S, Su, C, Zhang, H, Altman, NS, Schuster, SC, Timko, MP, Yoder, JI, Westwood, JH & Depamphilis, CW 2016, 'Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 45, pp. E7010-E7019. https://doi.org/10.1073/pnas.1608765113

Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation. / Yang, Zhenzhen; Zhang, Yeting; Wafula, Eric K.; Honaas, Loren A.; Ralph, Paula E.; Jones, Sam; Clarke, Christopher R.; Liu, Siming; Su, Chun; Zhang, Huiting; Altman, Naomi S.; Schuster, Stephan C.; Timko, Michael P.; Yoder, John I.; Westwood, James H.; Depamphilis, Claude Walker.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 45, 08.11.2016, p. E7010-E7019.

Research output: Contribution to journalArticle

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T1 - Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

AU - Yang, Zhenzhen

AU - Zhang, Yeting

AU - Wafula, Eric K.

AU - Honaas, Loren A.

AU - Ralph, Paula E.

AU - Jones, Sam

AU - Clarke, Christopher R.

AU - Liu, Siming

AU - Su, Chun

AU - Zhang, Huiting

AU - Altman, Naomi S.

AU - Schuster, Stephan C.

AU - Timko, Michael P.

AU - Yoder, John I.

AU - Westwood, James H.

AU - Depamphilis, Claude Walker

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N2 - Horizontal 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 highconfidence 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.

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