Paper · 2007 · BMC Evolutionary Biology

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; et al.

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verbatim quotes
255
citations
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research areas
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Open access · cc-by

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.

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Claims 9

Observationobservedoriginal resultmeasured

Claim · model-written summary

The mitochondrial phylogeny agrees with independent studies of non-parasitic plant relationships.

Taxon
angiospermsMagnoliopsidat0
Outcome
mtDNA phylogeny agrees with independent studiese0
Comparator
independent studiese0

Verbatim

e0

“the mtDNA phylogeny agrees with independent studies in terms of non-parasitic plant relationships”

✓ located verbatim in the source · abstract, characters 601–698 · show in text ↑
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“angiosperms”

✓ located verbatim in the source · title, characters 64–75 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Mitochondrial phylogeny indicates at least 11 independent origins of parasitism in angiosperms.

Taxon
angiospermsMagnoliopsidat0
Outcome
independent origins of parasitisme0
Value
at least 11e0

Verbatim

e0

“reveals at least 11 independent origins of parasitism in angiosperms”

✓ located verbatim in the source · abstract, characters 703–771 · show in text ↑
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“angiosperms”

✓ located verbatim in the source · title, characters 64–75 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Eight of the origins comprise entirely holoparasitic species lacking photosynthesis.

Taxon
angiospermsMagnoliopsidat0
Outcome
holoparasitic species that lack photosynthetic abilitye0
Value
eighte0

Verbatim

e0

“eight of which consist entirely of holoparasitic species that lack photosynthetic ability”

✓ located verbatim in the source · abstract, characters 773–862 · show in text ↑
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“angiosperms”

✓ located verbatim in the source · title, characters 64–75 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

Modern parasites appear to have evolved disproportionately in certain lineages.

Taxon
parasitic plantst0
Outcome
disproportionately evolved in certain lineagese0

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e0

“modern-day parasites have disproportionately evolved in certain lineages”

✓ located verbatim in the source · abstract, characters 908–980 · show in text ↑
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“parasitic plants”

✓ located verbatim in the source · title, characters 109–125 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

Endoparasitism arose convergently in four clades.

Taxon
parasitic plantst0
Outcome
endoparasitic habit has arisen by convergencee0
Value
four cladese0

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e0

“the endoparasitic habit has arisen by convergence in four clades”

✓ located verbatim in the source · abstract, characters 990–1054 · show in text ↑
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“parasitic plants”

✓ located verbatim in the source · title, characters 109–125 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Single-gene analyses reveal multiple horizontal transfers of atp1 from hosts to parasite lineages.

Taxon
parasitic plantst0
Interactor
hoste0host
Gene
atp1e0
Outcome
multiple horizontal transfers of atp1 from host to parasite lineagee0

Verbatim

e0

“reduced taxon, single gene analyses revealed multiple horizontal transfers of atp1 from host to parasite lineage”

✓ located verbatim in the source · abstract, characters 1069–1181 · show in text ↑
t0

“parasitic plants”

✓ located verbatim in the source · title, characters 109–125 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

A chimeric atp1 sequence supports recent host-to-parasite transfer in Pilostyles and multiple historical xenolog acquisitions.

Taxon
PilostylesPilostylese0
Interactor
hoste0host
Gene
atp1e0
Outcome
recent host-to-parasite atp1 transfere0
Qualifier
multiple historical xenologous gene acquisitionse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Pilostyles
Pilostyles · Taxon · picture of the genus (one of its species)Kevin Thiele from Perth, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“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”

✓ located verbatim in the source · abstract, characters 1291–1498 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Origins of parasitism are strongly correlated with horizontal acquisitions of the invasive coxI group I intron.

Taxon
angiospermsMagnoliopsidat0
Gene
coxI group I introne0
Outcome
origins of parasitisme0

Not reportedDirection

Verbatim

e0

“the origins of parasitism in angiosperms are strongly correlated with horizontal acquisitions of the invasive coxI group I intron”

✓ located verbatim in the source · abstract, characters 1577–1706 · show in text ↑
t0

“angiosperms”

✓ located verbatim in the source · title, characters 64–75 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors infer that parasites may vector horizontal gene transfer in angiosperms.

Taxon
angiospermsMagnoliopsidat0
Outcome
horizontal gene transfere0
Qualifier
parasites may be important vectorse0

Verbatim

e0

“suggesting that parasites may be important vectors of horizontal gene transfer in angiosperms”

✓ located verbatim in the source · abstract, characters 1183–1276 · show in text ↑
t0

“angiosperms”

✓ located verbatim in the source · title, characters 64–75 · show in text ↑