Polyploidy Did Not Predate the Evolution of Nodulation in All Legumes

Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining t...

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Published inPloS one Vol. 5; no. 7; p. e11630
Main Authors Cannon, Steven B, Ilut, Dan, Farmer, Andrew D, Maki, Sonja L, May, Gregory D, Singer, Susan R, Doyle, Jeff J, Shiu, Shin-Han
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 16.07.2010
Public Library of Science (PLoS)
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Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0011630

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Abstract Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias) – which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes. Using transcriptome sequence data from Chamaecrista fasciculata , a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata , Glycine max (soybean), Medicago truncatula , and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation. The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
AbstractList Background Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias) – which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes. Methodology/Principal Findings Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation. Conclusions The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias) - which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes. Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation. The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias)--which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes.BACKGROUNDSeveral lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias)--which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes.Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation.METHODOLOGY/PRINCIPAL FINDINGSUsing transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation.The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.CONCLUSIONSThe ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias)--which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes. Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation. The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
Background Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known whether this event was confined to the papilionoid subfamily (Papilionoideae; e.g. beans, medics, lupins) or occurred earlier. Determining the timing of the polyploidy event is important for understanding whether polyploidy might have contributed to rapid diversification and radiation of the legumes near the origin of the family; and whether polyploidy might have provided genetic material that enabled the evolution of a novel organ, the nitrogen-fixing nodule. Although symbioses with nitrogen-fixing partners have evolved in several lineages in the rosid I clade, nodules are widespread only in legume taxa, being nearly universal in the papilionoids and in the mimosoid subfamily (e.g., mimosas, acacias) – which diverged from the papilionoid legumes around 58 million years ago, soon after the origin of the legumes. Methodology/Principal Findings Using transcriptome sequence data from Chamaecrista fasciculata, a nodulating member of the mimosoid clade, we tested whether this species underwent polyploidy within the timeframe of legume diversification. Analysis of gene family branching orders and synonymous-site divergence data from C. fasciculata, Glycine max (soybean), Medicago truncatula, and Vitis vinifera (grape; an outgroup to the rosid taxa) establish that the polyploidy event known from soybean and Medicago occurred after the separation of the mimosoid and papilionoid clades, and at or shortly before the Papilionoideae radiation. Conclusions The ancestral legume genome was not fundamentally polyploid. Moreover, because there has not been an independent instance of polyploidy in the Chamaecrista lineage there is no necessary connection between polyploidy and nodulation in legumes. Chamaecrista may serve as a useful model in the legumes that lacks a paleopolyploid history, at least relative to the widely studied papilionoid models.
Audience Academic
Author Cannon, Steven B
Ilut, Dan
Singer, Susan R
Maki, Sonja L
Doyle, Jeff J
Farmer, Andrew D
Shiu, Shin-Han
May, Gregory D
AuthorAffiliation 1 United States Department of Agriculture-Agricultural Research Service, Corn Insects and Crop Genomics Research Unit, Iowa State University, Ames, Iowa, United States of America
Michigan State University, United States of America
3 National Center for Genome Resources, Santa Fe, New Mexico, United States of America
4 Department of Biology, Carleton College, Northfield, Minnesota, United States of America
2 Department of Plant Biology, Cornell University, Ithaca, New York, United States of America
AuthorAffiliation_xml – name: 2 Department of Plant Biology, Cornell University, Ithaca, New York, United States of America
– name: Michigan State University, United States of America
– name: 1 United States Department of Agriculture-Agricultural Research Service, Corn Insects and Crop Genomics Research Unit, Iowa State University, Ames, Iowa, United States of America
– name: 3 National Center for Genome Resources, Santa Fe, New Mexico, United States of America
– name: 4 Department of Biology, Carleton College, Northfield, Minnesota, United States of America
Author_xml – sequence: 1
  fullname: Cannon, Steven B
– sequence: 2
  fullname: Ilut, Dan
– sequence: 3
  fullname: Farmer, Andrew D
– sequence: 4
  fullname: Maki, Sonja L
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  fullname: May, Gregory D
– sequence: 6
  fullname: Singer, Susan R
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  fullname: Doyle, Jeff J
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  fullname: Shiu, Shin-Han
BackLink https://www.ncbi.nlm.nih.gov/pubmed/20661290$$D View this record in MEDLINE/PubMed
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Conceived and designed the experiments: SBC SS JD. Performed the experiments: SLM. Analyzed the data: SBC DI ADF. Contributed reagents/materials/analysis tools: GM SS. Wrote the paper: SBC JD.
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Snippet Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not been known...
Background Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not...
BACKGROUND: Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has...
Background Several lines of evidence indicate that polyploidy occurred by around 54 million years ago, early in the history of legume evolution, but it has not...
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SubjectTerms Acacia
Alfalfa
Analysis
Beans
Biological evolution
Chamaecrista fasciculata
Deoxyribonucleic acid
Divergence
Diversification
DNA
Evolution
Evolution, Molecular
Fabaceae - classification
Fabaceae - genetics
Gene expression
Genes
Genetic engineering
Genetic research
Genome, Plant - genetics
Genomes
Genomics
Glycine
Glycine max
grapes
Legumes
Lupins
Medicago truncatula
Mutation
Nitrogen fixation
Nodulation
Nodules
Papilionoideae
Phylogenetics
Phylogeny
Plant biology
Plant Biology/Plant Genetics and Gene Expression
Plant Biology/Plant Genomes and Evolution
Plant Biology/Plant Growth and Development
Polyploidy
Radiation
Raw materials
Soybeans
Symbiosis
Taxa
Taxonomy
transcriptome
Vitis vinifera
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Title Polyploidy Did Not Predate the Evolution of Nodulation in All Legumes
URI https://www.ncbi.nlm.nih.gov/pubmed/20661290
https://www.proquest.com/docview/1292425518
https://www.proquest.com/docview/2000011831
https://www.proquest.com/docview/734033544
https://pubmed.ncbi.nlm.nih.gov/PMC2905438
https://doaj.org/article/bbb444fe90464b55b62659cfde184ddf
http://dx.doi.org/10.1371/journal.pone.0011630
Volume 5
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