Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.

Genetic analyses of plant symbiotic mutants has led to the identification of key genes involved in Rhizobium-legume communication as well as in development and function of nitrogen fixing root nodules. However, the impact of these genes in coordinating the transcriptional programs of nodule developm...

Full description

Bibliographic Details
Main Authors: Niels Høgslund, Simona Radutoiu, Lene Krusell, Vera Voroshilova, Matthew A Hannah, Nicolas Goffard, Diego H Sanchez, Felix Lippold, Thomas Ott, Shusei Sato, Satoshi Tabata, Poul Liboriussen, Gitte V Lohmann, Leif Schauser, Georg F Weiller, Michael K Udvardi, Jens Stougaard
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-08-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2717213?pdf=render
id doaj-75784289428e4fc8a37f70063014bbdf
record_format Article
spelling doaj-75784289428e4fc8a37f70063014bbdf2020-11-24T21:34:05ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-08-0148e655610.1371/journal.pone.0006556Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.Niels HøgslundSimona RadutoiuLene KrusellVera VoroshilovaMatthew A HannahNicolas GoffardDiego H SanchezFelix LippoldThomas OttShusei SatoSatoshi TabataPoul LiboriussenGitte V LohmannLeif SchauserGeorg F WeillerMichael K UdvardiJens StougaardGenetic analyses of plant symbiotic mutants has led to the identification of key genes involved in Rhizobium-legume communication as well as in development and function of nitrogen fixing root nodules. However, the impact of these genes in coordinating the transcriptional programs of nodule development has only been studied in limited and isolated studies. Here, we present an integrated genome-wide analysis of transcriptome landscapes in Lotus japonicus wild-type and symbiotic mutant plants. Encompassing five different organs, five stages of the sequentially developed determinate Lotus root nodules, and eight mutants impaired at different stages of the symbiotic interaction, our data set integrates an unprecedented combination of organ- or tissue-specific profiles with mutant transcript profiles. In total, 38 different conditions sampled under the same well-defined growth regimes were included. This comprehensive analysis unravelled new and unexpected patterns of transcriptional regulation during symbiosis and organ development. Contrary to expectations, none of the previously characterized nodulins were among the 37 genes specifically expressed in nodules. Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced. A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection. Combining wild type and mutant profiles of these transcripts demonstrates the activation of a complex genetic program that delineates symbiotic nitrogen fixation. The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.http://europepmc.org/articles/PMC2717213?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Niels Høgslund
Simona Radutoiu
Lene Krusell
Vera Voroshilova
Matthew A Hannah
Nicolas Goffard
Diego H Sanchez
Felix Lippold
Thomas Ott
Shusei Sato
Satoshi Tabata
Poul Liboriussen
Gitte V Lohmann
Leif Schauser
Georg F Weiller
Michael K Udvardi
Jens Stougaard
spellingShingle Niels Høgslund
Simona Radutoiu
Lene Krusell
Vera Voroshilova
Matthew A Hannah
Nicolas Goffard
Diego H Sanchez
Felix Lippold
Thomas Ott
Shusei Sato
Satoshi Tabata
Poul Liboriussen
Gitte V Lohmann
Leif Schauser
Georg F Weiller
Michael K Udvardi
Jens Stougaard
Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
PLoS ONE
author_facet Niels Høgslund
Simona Radutoiu
Lene Krusell
Vera Voroshilova
Matthew A Hannah
Nicolas Goffard
Diego H Sanchez
Felix Lippold
Thomas Ott
Shusei Sato
Satoshi Tabata
Poul Liboriussen
Gitte V Lohmann
Leif Schauser
Georg F Weiller
Michael K Udvardi
Jens Stougaard
author_sort Niels Høgslund
title Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
title_short Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
title_full Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
title_fullStr Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
title_full_unstemmed Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
title_sort dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2009-08-01
description Genetic analyses of plant symbiotic mutants has led to the identification of key genes involved in Rhizobium-legume communication as well as in development and function of nitrogen fixing root nodules. However, the impact of these genes in coordinating the transcriptional programs of nodule development has only been studied in limited and isolated studies. Here, we present an integrated genome-wide analysis of transcriptome landscapes in Lotus japonicus wild-type and symbiotic mutant plants. Encompassing five different organs, five stages of the sequentially developed determinate Lotus root nodules, and eight mutants impaired at different stages of the symbiotic interaction, our data set integrates an unprecedented combination of organ- or tissue-specific profiles with mutant transcript profiles. In total, 38 different conditions sampled under the same well-defined growth regimes were included. This comprehensive analysis unravelled new and unexpected patterns of transcriptional regulation during symbiosis and organ development. Contrary to expectations, none of the previously characterized nodulins were among the 37 genes specifically expressed in nodules. Another surprise was the extensive transcriptional response in whole root compared to the susceptible root zone where the cellular response is most pronounced. A large number of transcripts predicted to encode transcriptional regulators, receptors and proteins involved in signal transduction, as well as many genes with unknown function, were found to be regulated during nodule organogenesis and rhizobial infection. Combining wild type and mutant profiles of these transcripts demonstrates the activation of a complex genetic program that delineates symbiotic nitrogen fixation. The complete data set was organized into an indexed expression directory that is accessible from a resource database, and here we present selected examples of biological questions that can be addressed with this comprehensive and powerful gene expression data set.
url http://europepmc.org/articles/PMC2717213?pdf=render
work_keys_str_mv AT nielshøgslund dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT simonaradutoiu dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT lenekrusell dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT veravoroshilova dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT matthewahannah dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT nicolasgoffard dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT diegohsanchez dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT felixlippold dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT thomasott dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT shuseisato dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT satoshitabata dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT poulliboriussen dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT gittevlohmann dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT leifschauser dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT georgfweiller dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT michaelkudvardi dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
AT jensstougaard dissectionofsymbiosisandorgandevelopmentbyintegratedtranscriptomeanalysisoflotusjaponicusmutantandwildtypeplants
_version_ 1725950564283449344