Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses

R. van Velzen, R. Holmer, F. Bu, L.J.J. Rutten, A.L. van Zeijl, W. Liu, L. Santuari, Q. Cao, Trupti Sharma, Defeng Shen, Yuda Purwana Roswanjaya, T. Wardhani, M. Seifi Kalhor, Joelle Jansen, D.J. van den Hoogen, Berivan Güngör, M.V. Hartog, J. Hontelez, Jan Verver, Wei-Cai Yang & 11 others E.G.W.M. Schijlen, Rimi Repin, M. Schilthuizen, M.E. Schranz, R. Heidstra, Kana Miyata, E. Fedorova, W. Kohlen, A.H.J. Bisseling, S. Smit, R. Geurts

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22 Citations (Scopus)

Abstract

Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.
LanguageEnglish
PagesE4700-E4709
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number20
Early online date1 May 2018
DOIs
Publication statusPublished - 15 May 2018

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Parasponia
Rhizobium
symbiosis
nodulation
genomics
nitrogen
legumes
Cannabaceae
Trema
microsymbionts
Frankia
genetic traits
genes
Medicago truncatula
Actinobacteria
organogenesis
transcriptomics
molecular genetics
engineering
ancestry

Cite this

van Velzen, R. ; Holmer, R. ; Bu, F. ; Rutten, L.J.J. ; van Zeijl, A.L. ; Liu, W. ; Santuari, L. ; Cao, Q. ; Sharma, Trupti ; Shen, Defeng ; Purwana Roswanjaya, Yuda ; Wardhani, T. ; Seifi Kalhor, M. ; Jansen, Joelle ; van den Hoogen, D.J. ; Güngör, Berivan ; Hartog, M.V. ; Hontelez, J. ; Verver, Jan ; Yang, Wei-Cai ; Schijlen, E.G.W.M. ; Repin, Rimi ; Schilthuizen, M. ; Schranz, M.E. ; Heidstra, R. ; Miyata, Kana ; Fedorova, E. ; Kohlen, W. ; Bisseling, A.H.J. ; Smit, S. ; Geurts, R. / Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 20. pp. E4700-E4709.
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title = "Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses",
abstract = "Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.",
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Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. / van Velzen, R.; Holmer, R.; Bu, F.; Rutten, L.J.J.; van Zeijl, A.L.; Liu, W.; Santuari, L.; Cao, Q.; Sharma, Trupti; Shen, Defeng; Purwana Roswanjaya, Yuda; Wardhani, T.; Seifi Kalhor, M.; Jansen, Joelle; van den Hoogen, D.J.; Güngör, Berivan; Hartog, M.V.; Hontelez, J.; Verver, Jan; Yang, Wei-Cai; Schijlen, E.G.W.M.; Repin, Rimi; Schilthuizen, M.; Schranz, M.E.; Heidstra, R.; Miyata, Kana; Fedorova, E.; Kohlen, W.; Bisseling, A.H.J.; Smit, S.; Geurts, R.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 20, 15.05.2018, p. E4700-E4709.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses

AU - van Velzen, R.

AU - Holmer, R.

AU - Bu, F.

AU - Rutten, L.J.J.

AU - van Zeijl, A.L.

AU - Liu, W.

AU - Santuari, L.

AU - Cao, Q.

AU - Sharma, Trupti

AU - Shen, Defeng

AU - Purwana Roswanjaya, Yuda

AU - Wardhani, T.

AU - Seifi Kalhor, M.

AU - Jansen, Joelle

AU - van den Hoogen, D.J.

AU - Güngör, Berivan

AU - Hartog, M.V.

AU - Hontelez, J.

AU - Verver, Jan

AU - Yang, Wei-Cai

AU - Schijlen, E.G.W.M.

AU - Repin, Rimi

AU - Schilthuizen, M.

AU - Schranz, M.E.

AU - Heidstra, R.

AU - Miyata, Kana

AU - Fedorova, E.

AU - Kohlen, W.

AU - Bisseling, A.H.J.

AU - Smit, S.

AU - Geurts, R.

PY - 2018/5/15

Y1 - 2018/5/15

N2 - Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.

AB - Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.

U2 - 10.1073/pnas.1721395115

DO - 10.1073/pnas.1721395115

M3 - Article

VL - 115

SP - E4700-E4709

JO - Proceedings of the National Academy of Sciences of the United States of America

T2 - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

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