Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages

Julia Naumann, Karsten Salomo, Joshua P. Der, Eric K. Wafula, Jay F. Bolin, Erika Maass, Lena Frenzke, Marie Stéphanie Samain, Christoph Neinhuis, Claude W. DePamphilis, Stefan Wanke

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the "strangest plants in the world", Hydnora visseri (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the "temporal specialization hypothesis" (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.

Original languageEnglish (US)
Article numbere79204
JournalPloS one
Volume8
Issue number11
DOIs
StatePublished - Nov 12 2013

Fingerprint

Piperales
Aristolochiaceae
Angiosperms
Angiospermae
Genes
Balanophoraceae
Parasites
Plastid Genomes
Plant Genes
phylogeny
Santalales
Plastids
genes
Photosynthesis
Clocks
Transcriptome
parasites
parasitic plants
transcriptome
Biodiversity

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

Naumann, Julia ; Salomo, Karsten ; Der, Joshua P. ; Wafula, Eric K. ; Bolin, Jay F. ; Maass, Erika ; Frenzke, Lena ; Samain, Marie Stéphanie ; Neinhuis, Christoph ; DePamphilis, Claude W. ; Wanke, Stefan. / Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages. In: PloS one. 2013 ; Vol. 8, No. 11.
@article{6ee719db832a422db15587a27ecf3be3,
title = "Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages",
abstract = "Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the {"}strangest plants in the world{"}, Hydnora visseri (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the {"}temporal specialization hypothesis{"} (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.",
author = "Julia Naumann and Karsten Salomo and Der, {Joshua P.} and Wafula, {Eric K.} and Bolin, {Jay F.} and Erika Maass and Lena Frenzke and Samain, {Marie St{\'e}phanie} and Christoph Neinhuis and DePamphilis, {Claude W.} and Stefan Wanke",
year = "2013",
month = "11",
day = "12",
doi = "10.1371/journal.pone.0079204",
language = "English (US)",
volume = "8",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "11",

}

Naumann, J, Salomo, K, Der, JP, Wafula, EK, Bolin, JF, Maass, E, Frenzke, L, Samain, MS, Neinhuis, C, DePamphilis, CW & Wanke, S 2013, 'Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages', PloS one, vol. 8, no. 11, e79204. https://doi.org/10.1371/journal.pone.0079204

Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages. / Naumann, Julia; Salomo, Karsten; Der, Joshua P.; Wafula, Eric K.; Bolin, Jay F.; Maass, Erika; Frenzke, Lena; Samain, Marie Stéphanie; Neinhuis, Christoph; DePamphilis, Claude W.; Wanke, Stefan.

In: PloS one, Vol. 8, No. 11, e79204, 12.11.2013.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Single-copy nuclear genes place haustorial Hydnoraceae within piperales and reveal a Cretaceous origin of multiple parasitic angiosperm lineages

AU - Naumann, Julia

AU - Salomo, Karsten

AU - Der, Joshua P.

AU - Wafula, Eric K.

AU - Bolin, Jay F.

AU - Maass, Erika

AU - Frenzke, Lena

AU - Samain, Marie Stéphanie

AU - Neinhuis, Christoph

AU - DePamphilis, Claude W.

AU - Wanke, Stefan

PY - 2013/11/12

Y1 - 2013/11/12

N2 - Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the "strangest plants in the world", Hydnora visseri (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the "temporal specialization hypothesis" (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.

AB - Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the "strangest plants in the world", Hydnora visseri (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the "temporal specialization hypothesis" (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.

UR - http://www.scopus.com/inward/record.url?scp=84893379162&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84893379162&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0079204

DO - 10.1371/journal.pone.0079204

M3 - Article

C2 - 24265760

AN - SCOPUS:84893379162

VL - 8

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 11

M1 - e79204

ER -