Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants

Todd J. Barkman, Joel R. McNeal, Seok Hong Lim, Gwen Coat, Henrietta B. Croom, Nelson D. Young, Claude Walker Depamphilis

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141 Citations (Scopus)

Abstract

Background. Some of the most difficult phylogenetic questions in evolutionary biology involve identification of the free-living relatives of parasitic organisms, particularly those of parasitic flowering plants. Consequently, the number of origins of parasitism and the phylogenetic distribution of the heterotrophic lifestyle among angiosperm lineages is unclear. Results. Here we report the results of a phylogenetic analysis of 102 species of seed plants designed to infer the position of all haustorial parasitic angiosperm lineages using three mitochondrial genes: atp1, coxI, and matR. Overall, the mtDNA phylogeny agrees with independent studies in terms of non-parasitic plant relationships and reveals at least 11 independent origins of parasitism in angiosperms, eight of which consist entirely of holoparasitic species that lack photosynthetic ability. From these results, it can be inferred that modern-day parasites have disproportionately evolved in certain lineages and that the endoparasitic habit has arisen by convergence in four clades. In addition, reduced taxon, single gene analyses revealed multiple horizontal transfers of atp1 from host to parasite lineage, suggesting that parasites may be important vectors of horizontal gene transfer in angiosperms. Furthermore, in Pilostyles we show evidence for a recent host-to-parasite atp1 transfer based on a chimeric gene sequence that indicates multiple historical xenologous gene acquisitions have occurred in this endoparasite. Finally, the phylogenetic relationships inferred for parasites indicate that the origins of parasitism in angiosperms are strongly correlated with horizontal acquisitions of the invasive coxI group I intron. Conclusion. Collectively, these results indicate that the parasitic lifestyle has arisen repeatedly in angiosperm evolutionary history and results in increasing parasite genomic chimerism over time.

Original languageEnglish (US)
Article number248
JournalBMC Evolutionary Biology
Volume7
Issue number1
DOIs
StatePublished - Dec 1 2007

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Angiosperms
parasitic plant
Chimerism
parasitic plants
chimerism
Mitochondrial DNA
parasitism
angiosperm
mitochondrial DNA
Angiospermae
genomics
Parasites
parasite
parasites
phylogeny
phylogenetics
gene
Life Style
lifestyle
Genes

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics

Cite this

Barkman, Todd J. ; McNeal, Joel R. ; Lim, Seok Hong ; Coat, Gwen ; Croom, Henrietta B. ; Young, Nelson D. ; Depamphilis, Claude Walker. / Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. In: BMC Evolutionary Biology. 2007 ; Vol. 7, No. 1.
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Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. / Barkman, Todd J.; McNeal, Joel R.; Lim, Seok Hong; Coat, Gwen; Croom, Henrietta B.; Young, Nelson D.; Depamphilis, Claude Walker.

In: BMC Evolutionary Biology, Vol. 7, No. 1, 248, 01.12.2007.

Research output: Contribution to journalArticle

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AU - Depamphilis, Claude Walker

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AB - Background. Some of the most difficult phylogenetic questions in evolutionary biology involve identification of the free-living relatives of parasitic organisms, particularly those of parasitic flowering plants. Consequently, the number of origins of parasitism and the phylogenetic distribution of the heterotrophic lifestyle among angiosperm lineages is unclear. Results. Here we report the results of a phylogenetic analysis of 102 species of seed plants designed to infer the position of all haustorial parasitic angiosperm lineages using three mitochondrial genes: atp1, coxI, and matR. Overall, the mtDNA phylogeny agrees with independent studies in terms of non-parasitic plant relationships and reveals at least 11 independent origins of parasitism in angiosperms, eight of which consist entirely of holoparasitic species that lack photosynthetic ability. From these results, it can be inferred that modern-day parasites have disproportionately evolved in certain lineages and that the endoparasitic habit has arisen by convergence in four clades. In addition, reduced taxon, single gene analyses revealed multiple horizontal transfers of atp1 from host to parasite lineage, suggesting that parasites may be important vectors of horizontal gene transfer in angiosperms. Furthermore, in Pilostyles we show evidence for a recent host-to-parasite atp1 transfer based on a chimeric gene sequence that indicates multiple historical xenologous gene acquisitions have occurred in this endoparasite. Finally, the phylogenetic relationships inferred for parasites indicate that the origins of parasitism in angiosperms are strongly correlated with horizontal acquisitions of the invasive coxI group I intron. Conclusion. Collectively, these results indicate that the parasitic lifestyle has arisen repeatedly in angiosperm evolutionary history and results in increasing parasite genomic chimerism over time.

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