Co-option of pre-existing pathways during Rhizobium-legume symbiosis evolution

A. Lillo

Research output: Thesisinternal PhD, WUAcademic

Abstract

Fixed nitrogen is one of the most limiting factors for plant growth. One of the most important nitrogen-fixing systems is the rhizobium root nodule symbiosis. In this Thesis I have studied the legume-rhizobium symbiosis, starting from the idea that part of pre-existing signalling pathways have been co-opted during evolution of this mutualistic interaction. Gene duplications -of which a whole genome duplication (WGD) is the most dramatic variant- are known as important driving forces in evolution of new traits. 56 to 65 million years ago an ancestral legume species within the Papilionoidae subfamily (Papilionoids) experienced a WGD event and subsequently gave rise to several major phylogenetic crowns. I hypothesize that among the orthologous gene pairs maintained are genes that are essential for nodulation. I adopted a phylogenetic strategy to identify new candidate genes involved in the legume-Rhizobium symbiosis
In a targeted approach, we focussed on the cytokinin phosphorelay pathway. This resulted in the identification of one gene pair encoding type-A Response Regulators (RRs) with a positive regulatory role for these proteins in root nodule formation. Yet the illustrated role for MtRR9 and MtRR11 in rhizobial symbiosis provides a proof of principle of this method to identify gene pairs involved in legume specific characters. An unbiased search for paralogous gene pairs revealed two conserved gene duplications in the NADPH oxidases gene family. NADPH oxidases are reactive oxygen species (ROS) producing enzymes. We identified two sets of duplicated genes that have been maintained after the Papilionoid specific WGD and we show that MtRBOHA and MtRBOHG are redundant, yet essential during symbiosis.
Moreover, although it is commonly believed that exclusively pericycle cells give rise to the lateral root primordium, similar as seen in Arabidopsis thaliana, we provide morphological evidence that in the studied legume species this is not the case. In both, Lotus and Medicago, also root cortical cell divisions occur during lateral root formation. Furthermore, we found a striking correlation in the cell layers that are recruited during lateral root and nodule primordium formation. This supports the hypothesis that at least parts of the lateral root developmental program have been recruited during evolution of symbiotic root nodules.
 

Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Wageningen University
Supervisors/Advisors
  • Bisseling, Ton, Promotor
  • Geurts, Rene, Co-promotor
Award date5 Sep 2012
Place of PublicationS.l.
Publisher
Print ISBNs9789461733443
Publication statusPublished - 2012

Fingerprint

Rhizobium
symbiosis
legumes
root nodules
genes
gene duplication
genome
root primordia
Medicago
Lotus
phylogeny
nitrogen
nodulation
plant growth substances
cytokinins
tree crown
cell division
reactive oxygen species
Arabidopsis thaliana
cells

Keywords

  • rhizobium
  • fabaceae
  • symbiosis
  • evolution
  • nitrogen fixation
  • roots
  • phylogenetics
  • genomes
  • medicago
  • root primordia

Cite this

@phdthesis{8721a5aa01554a638bbdc0075a6ba469,
title = "Co-option of pre-existing pathways during Rhizobium-legume symbiosis evolution",
abstract = "Fixed nitrogen is one of the most limiting factors for plant growth. One of the most important nitrogen-fixing systems is the rhizobium root nodule symbiosis. In this Thesis I have studied the legume-rhizobium symbiosis, starting from the idea that part of pre-existing signalling pathways have been co-opted during evolution of this mutualistic interaction. Gene duplications -of which a whole genome duplication (WGD) is the most dramatic variant- are known as important driving forces in evolution of new traits. 56 to 65 million years ago an ancestral legume species within the Papilionoidae subfamily (Papilionoids) experienced a WGD event and subsequently gave rise to several major phylogenetic crowns. I hypothesize that among the orthologous gene pairs maintained are genes that are essential for nodulation. I adopted a phylogenetic strategy to identify new candidate genes involved in the legume-Rhizobium symbiosis In a targeted approach, we focussed on the cytokinin phosphorelay pathway. This resulted in the identification of one gene pair encoding type-A Response Regulators (RRs) with a positive regulatory role for these proteins in root nodule formation. Yet the illustrated role for MtRR9 and MtRR11 in rhizobial symbiosis provides a proof of principle of this method to identify gene pairs involved in legume specific characters. An unbiased search for paralogous gene pairs revealed two conserved gene duplications in the NADPH oxidases gene family. NADPH oxidases are reactive oxygen species (ROS) producing enzymes. We identified two sets of duplicated genes that have been maintained after the Papilionoid specific WGD and we show that MtRBOHA and MtRBOHG are redundant, yet essential during symbiosis. Moreover, although it is commonly believed that exclusively pericycle cells give rise to the lateral root primordium, similar as seen in Arabidopsis thaliana, we provide morphological evidence that in the studied legume species this is not the case. In both, Lotus and Medicago, also root cortical cell divisions occur during lateral root formation. Furthermore, we found a striking correlation in the cell layers that are recruited during lateral root and nodule primordium formation. This supports the hypothesis that at least parts of the lateral root developmental program have been recruited during evolution of symbiotic root nodules.  ",
keywords = "rhizobium, fabaceae, symbiose, evolutie, stikstoffixatie, wortels, fylogenetica, genomen, medicago, eerste wortels, rhizobium, fabaceae, symbiosis, evolution, nitrogen fixation, roots, phylogenetics, genomes, medicago, root primordia",
author = "A. Lillo",
note = "WU thesis 5282",
year = "2012",
language = "English",
isbn = "9789461733443",
publisher = "s.n.",
school = "Wageningen University",

}

Lillo, A 2012, 'Co-option of pre-existing pathways during Rhizobium-legume symbiosis evolution', Doctor of Philosophy, Wageningen University, S.l..

Co-option of pre-existing pathways during Rhizobium-legume symbiosis evolution. / Lillo, A.

S.l. : s.n., 2012. 151 p.

Research output: Thesisinternal PhD, WUAcademic

TY - THES

T1 - Co-option of pre-existing pathways during Rhizobium-legume symbiosis evolution

AU - Lillo, A.

N1 - WU thesis 5282

PY - 2012

Y1 - 2012

N2 - Fixed nitrogen is one of the most limiting factors for plant growth. One of the most important nitrogen-fixing systems is the rhizobium root nodule symbiosis. In this Thesis I have studied the legume-rhizobium symbiosis, starting from the idea that part of pre-existing signalling pathways have been co-opted during evolution of this mutualistic interaction. Gene duplications -of which a whole genome duplication (WGD) is the most dramatic variant- are known as important driving forces in evolution of new traits. 56 to 65 million years ago an ancestral legume species within the Papilionoidae subfamily (Papilionoids) experienced a WGD event and subsequently gave rise to several major phylogenetic crowns. I hypothesize that among the orthologous gene pairs maintained are genes that are essential for nodulation. I adopted a phylogenetic strategy to identify new candidate genes involved in the legume-Rhizobium symbiosis In a targeted approach, we focussed on the cytokinin phosphorelay pathway. This resulted in the identification of one gene pair encoding type-A Response Regulators (RRs) with a positive regulatory role for these proteins in root nodule formation. Yet the illustrated role for MtRR9 and MtRR11 in rhizobial symbiosis provides a proof of principle of this method to identify gene pairs involved in legume specific characters. An unbiased search for paralogous gene pairs revealed two conserved gene duplications in the NADPH oxidases gene family. NADPH oxidases are reactive oxygen species (ROS) producing enzymes. We identified two sets of duplicated genes that have been maintained after the Papilionoid specific WGD and we show that MtRBOHA and MtRBOHG are redundant, yet essential during symbiosis. Moreover, although it is commonly believed that exclusively pericycle cells give rise to the lateral root primordium, similar as seen in Arabidopsis thaliana, we provide morphological evidence that in the studied legume species this is not the case. In both, Lotus and Medicago, also root cortical cell divisions occur during lateral root formation. Furthermore, we found a striking correlation in the cell layers that are recruited during lateral root and nodule primordium formation. This supports the hypothesis that at least parts of the lateral root developmental program have been recruited during evolution of symbiotic root nodules.  

AB - Fixed nitrogen is one of the most limiting factors for plant growth. One of the most important nitrogen-fixing systems is the rhizobium root nodule symbiosis. In this Thesis I have studied the legume-rhizobium symbiosis, starting from the idea that part of pre-existing signalling pathways have been co-opted during evolution of this mutualistic interaction. Gene duplications -of which a whole genome duplication (WGD) is the most dramatic variant- are known as important driving forces in evolution of new traits. 56 to 65 million years ago an ancestral legume species within the Papilionoidae subfamily (Papilionoids) experienced a WGD event and subsequently gave rise to several major phylogenetic crowns. I hypothesize that among the orthologous gene pairs maintained are genes that are essential for nodulation. I adopted a phylogenetic strategy to identify new candidate genes involved in the legume-Rhizobium symbiosis In a targeted approach, we focussed on the cytokinin phosphorelay pathway. This resulted in the identification of one gene pair encoding type-A Response Regulators (RRs) with a positive regulatory role for these proteins in root nodule formation. Yet the illustrated role for MtRR9 and MtRR11 in rhizobial symbiosis provides a proof of principle of this method to identify gene pairs involved in legume specific characters. An unbiased search for paralogous gene pairs revealed two conserved gene duplications in the NADPH oxidases gene family. NADPH oxidases are reactive oxygen species (ROS) producing enzymes. We identified two sets of duplicated genes that have been maintained after the Papilionoid specific WGD and we show that MtRBOHA and MtRBOHG are redundant, yet essential during symbiosis. Moreover, although it is commonly believed that exclusively pericycle cells give rise to the lateral root primordium, similar as seen in Arabidopsis thaliana, we provide morphological evidence that in the studied legume species this is not the case. In both, Lotus and Medicago, also root cortical cell divisions occur during lateral root formation. Furthermore, we found a striking correlation in the cell layers that are recruited during lateral root and nodule primordium formation. This supports the hypothesis that at least parts of the lateral root developmental program have been recruited during evolution of symbiotic root nodules.  

KW - rhizobium

KW - fabaceae

KW - symbiose

KW - evolutie

KW - stikstoffixatie

KW - wortels

KW - fylogenetica

KW - genomen

KW - medicago

KW - eerste wortels

KW - rhizobium

KW - fabaceae

KW - symbiosis

KW - evolution

KW - nitrogen fixation

KW - roots

KW - phylogenetics

KW - genomes

KW - medicago

KW - root primordia

M3 - internal PhD, WU

SN - 9789461733443

PB - s.n.

CY - S.l.

ER -