A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny.

Defeng Shen; Ting Ting Xiao; Robin van Velzen; Olga Kulikova; Xiaoyun Gong; Rene Geurts; Katharina Pawlowski; Ton Bisseling

doi:10.1105/tpc.19.00739

A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny.

Defeng Shen, Ting Ting Xiao, Robin van Velzen, Olga Kulikova, Xiaoyun Gong, Rene Geurts, Katharina Pawlowski, Ton Bisseling

King Abdullah University of Science and Technology

Research output: Contribution to journal › Article › peer-review

24 Scopus citations

Abstract

Some plants can fix atmospheric nitrogen by hosting symbiotic diazotrophic rhizobia or Frankia bacteria in root organs, known as nodules. Such nodule symbiosis occurs in ten lineages in four taxonomic orders; Fabales, Fagales, Cucurbitales and Rosales, which collectively are known as the nitrogen-fixing clade (NFC). Based on differences in ontogeny and histology, nodules have been divided into two types: legume-type and actinorhizal-type nodules. The evolutionary relationship between these nodule types has been a long-standing enigma for molecular and evolutionary biologists. Recent phylogenomic studies on nodulating and non-nodulating species in the NFC indicated a shared evolutionary origin of the nodulation trait in all ten lineages. However, this hypothesis faces a conundrum that legume-type and actinorhizal-type nodules have been regarded as fundamentally different. Here, we analysed the actinorhizal-type nodules formed by Parasponia andersonii (Rosales) and Alnus glutinosa (Fagales), and found that their ontogeny is more similar to that of legume-type nodules (Fabales) than generally assumed. We also show that in Medicago truncatula a homeotic mutation in the co-transcriptional regulator encoding gene NODULE ROOT1 (MtNOOT1) converts a legume-type nodule into actinorhizal type. These experimental findings suggest that the two nodule types have a shared evolutionary origin.

Original language	English (US)
Pages (from-to)	tpc.00739.2019
Journal	The Plant Cell
DOIs	https://doi.org/10.1105/tpc.19.00739
State	Published - Apr 12 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Pascal Ratet for providing the Mtnoot1 seeds (tnk507 and NF2717) and Nik Geldner for providing the AtCASP1 promoter GUS fusion vector. We also thank Henk Hilhorst for providing access to the unpublished genome of Castanospermum australe and Wouter Kohlen for providing access to the unpublished transcriptome of Chamaecrista stricta. This research was supported by European Research Council (grant number ERC-2011-AdG294790) to TB, Swedish Research Council Vetenskapsrådet (grant number VR 2012-03061) to KP; an NWO-VICI grant (grant number 865.13.001) to RG; and China Scholarship Council (grant number 201306040120) to DS.

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10.1105/tpc.19.00739

https://repository.kaust.edu.sa/bitstream/10754/662517/1/A%20homeotic%20.pdf

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@article{48facf8e7945438081b3f024e120fce9,

title = "A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny.",

abstract = "Some plants can fix atmospheric nitrogen by hosting symbiotic diazotrophic rhizobia or Frankia bacteria in root organs, known as nodules. Such nodule symbiosis occurs in ten lineages in four taxonomic orders; Fabales, Fagales, Cucurbitales and Rosales, which collectively are known as the nitrogen-fixing clade (NFC). Based on differences in ontogeny and histology, nodules have been divided into two types: legume-type and actinorhizal-type nodules. The evolutionary relationship between these nodule types has been a long-standing enigma for molecular and evolutionary biologists. Recent phylogenomic studies on nodulating and non-nodulating species in the NFC indicated a shared evolutionary origin of the nodulation trait in all ten lineages. However, this hypothesis faces a conundrum that legume-type and actinorhizal-type nodules have been regarded as fundamentally different. Here, we analysed the actinorhizal-type nodules formed by Parasponia andersonii (Rosales) and Alnus glutinosa (Fagales), and found that their ontogeny is more similar to that of legume-type nodules (Fabales) than generally assumed. We also show that in Medicago truncatula a homeotic mutation in the co-transcriptional regulator encoding gene NODULE ROOT1 (MtNOOT1) converts a legume-type nodule into actinorhizal type. These experimental findings suggest that the two nodule types have a shared evolutionary origin.",

author = "Defeng Shen and Xiao, {Ting Ting} and Velzen, {Robin van} and Olga Kulikova and Xiaoyun Gong and Rene Geurts and Katharina Pawlowski and Ton Bisseling",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Pascal Ratet for providing the Mtnoot1 seeds (tnk507 and NF2717) and Nik Geldner for providing the AtCASP1 promoter GUS fusion vector. We also thank Henk Hilhorst for providing access to the unpublished genome of Castanospermum australe and Wouter Kohlen for providing access to the unpublished transcriptome of Chamaecrista stricta. This research was supported by European Research Council (grant number ERC-2011-AdG294790) to TB, Swedish Research Council Vetenskapsr{\aa}det (grant number VR 2012-03061) to KP; an NWO-VICI grant (grant number 865.13.001) to RG; and China Scholarship Council (grant number 201306040120) to DS.",

year = "2020",

month = apr,

day = "12",

doi = "10.1105/tpc.19.00739",

language = "English (US)",

pages = "tpc.00739.2019",

journal = "The Plant Cell",

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T1 - A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny.

AU - Shen, Defeng

AU - Xiao, Ting Ting

AU - Velzen, Robin van

AU - Kulikova, Olga

AU - Gong, Xiaoyun

AU - Geurts, Rene

AU - Pawlowski, Katharina

AU - Bisseling, Ton

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Pascal Ratet for providing the Mtnoot1 seeds (tnk507 and NF2717) and Nik Geldner for providing the AtCASP1 promoter GUS fusion vector. We also thank Henk Hilhorst for providing access to the unpublished genome of Castanospermum australe and Wouter Kohlen for providing access to the unpublished transcriptome of Chamaecrista stricta. This research was supported by European Research Council (grant number ERC-2011-AdG294790) to TB, Swedish Research Council Vetenskapsrådet (grant number VR 2012-03061) to KP; an NWO-VICI grant (grant number 865.13.001) to RG; and China Scholarship Council (grant number 201306040120) to DS.

PY - 2020/4/12

Y1 - 2020/4/12

N2 - Some plants can fix atmospheric nitrogen by hosting symbiotic diazotrophic rhizobia or Frankia bacteria in root organs, known as nodules. Such nodule symbiosis occurs in ten lineages in four taxonomic orders; Fabales, Fagales, Cucurbitales and Rosales, which collectively are known as the nitrogen-fixing clade (NFC). Based on differences in ontogeny and histology, nodules have been divided into two types: legume-type and actinorhizal-type nodules. The evolutionary relationship between these nodule types has been a long-standing enigma for molecular and evolutionary biologists. Recent phylogenomic studies on nodulating and non-nodulating species in the NFC indicated a shared evolutionary origin of the nodulation trait in all ten lineages. However, this hypothesis faces a conundrum that legume-type and actinorhizal-type nodules have been regarded as fundamentally different. Here, we analysed the actinorhizal-type nodules formed by Parasponia andersonii (Rosales) and Alnus glutinosa (Fagales), and found that their ontogeny is more similar to that of legume-type nodules (Fabales) than generally assumed. We also show that in Medicago truncatula a homeotic mutation in the co-transcriptional regulator encoding gene NODULE ROOT1 (MtNOOT1) converts a legume-type nodule into actinorhizal type. These experimental findings suggest that the two nodule types have a shared evolutionary origin.

AB - Some plants can fix atmospheric nitrogen by hosting symbiotic diazotrophic rhizobia or Frankia bacteria in root organs, known as nodules. Such nodule symbiosis occurs in ten lineages in four taxonomic orders; Fabales, Fagales, Cucurbitales and Rosales, which collectively are known as the nitrogen-fixing clade (NFC). Based on differences in ontogeny and histology, nodules have been divided into two types: legume-type and actinorhizal-type nodules. The evolutionary relationship between these nodule types has been a long-standing enigma for molecular and evolutionary biologists. Recent phylogenomic studies on nodulating and non-nodulating species in the NFC indicated a shared evolutionary origin of the nodulation trait in all ten lineages. However, this hypothesis faces a conundrum that legume-type and actinorhizal-type nodules have been regarded as fundamentally different. Here, we analysed the actinorhizal-type nodules formed by Parasponia andersonii (Rosales) and Alnus glutinosa (Fagales), and found that their ontogeny is more similar to that of legume-type nodules (Fabales) than generally assumed. We also show that in Medicago truncatula a homeotic mutation in the co-transcriptional regulator encoding gene NODULE ROOT1 (MtNOOT1) converts a legume-type nodule into actinorhizal type. These experimental findings suggest that the two nodule types have a shared evolutionary origin.

UR - http://hdl.handle.net/10754/662517

UR - http://www.plantcell.org/lookup/doi/10.1105/tpc.19.00739

U2 - 10.1105/tpc.19.00739

DO - 10.1105/tpc.19.00739

M3 - Article

C2 - 32276984

SN - 1040-4651

SP - tpc.00739.2019

JO - The Plant Cell

JF - The Plant Cell

ER -

A Homeotic Mutation Changes Legume Nodule Ontogeny into Actinorhizal-type Ontogeny.

Abstract

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