Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection

14-3-3 proteins are found in all eukaryotes where they act as regulators of diverse signalling pathways associated with a wide range of biological processes. In this study the functional characterization of the ZmGF14-6 gene encoding a maize 14-3-3 protein is reported. Gene expression analyses indic...

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Published in:Journal of experimental botany Vol. 63; no. 2; pp. 983 - 999
Main Authors: CAMPO, Sonia, PERIS-PERIS, Cristina, MONTESINOS, Laura, PENAS, Gisela, MESSEGUER, Joaquima, SAN SEGUNDO, Blanca
Format: Journal Article
Language:English
Published: Oxford Oxford University Press 01-01-2012
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Abstract 14-3-3 proteins are found in all eukaryotes where they act as regulators of diverse signalling pathways associated with a wide range of biological processes. In this study the functional characterization of the ZmGF14-6 gene encoding a maize 14-3-3 protein is reported. Gene expression analyses indicated that ZmGF14-6 is up-regulated by fungal infection and salt treatment in maize plants, whereas its expression is down-regulated by drought stress. It is reported that rice plants constitutively expressing ZmGF14-6 displayed enhanced tolerance to drought stress which was accompanied by a stronger induction of drought-associated rice genes. However, rice plants expressing ZmGF14-6 either in a constitutive or under a pathogen-inducible regime showed a higher susceptibility to infection by the fungal pathogens Fusarium verticillioides and Magnaporthe oryzae. Under infection conditions, a lower intensity in the expression of defence-related genes occurred in ZmGF14-6 rice plants. These findings support that ZmGF14-6 positively regulates drought tolerance in transgenic rice while negatively modulating the plant defence response to pathogen infection. Transient expression assays of fluorescently labelled ZmGF14-6 protein in onion epidermal cells revealed a widespread distribution of ZmGF14-6 in the cytoplasm and nucleus. Additionally, colocalization experiments of fluorescently labelled ZmGF14-6 with organelle markers, in combination with cell labelling with the endocytic tracer FM4-64, revealed a subcellular localization of ZmGF14-6 in the early endosomes. Taken together, these results improve our understanding of the role of ZmGF14-6 in stress signalling pathways, while indicating that ZmGF14-6 inversely regulates the plant response to biotic and abiotic stresses.
AbstractList 14-3-3 proteins are found in all eukaryotes where they act as regulators of diverse signalling pathways associated with a wide range of biological processes. In this study the functional characterization of the ZmGF14-6 gene encoding a maize 14-3-3 protein is reported. Gene expression analyses indicated that ZmGF14-6 is up-regulated by fungal infection and salt treatment in maize plants, whereas its expression is down-regulated by drought stress. It is reported that rice plants constitutively expressing ZmGF14-6 displayed enhanced tolerance to drought stress which was accompanied by a stronger induction of drought-associated rice genes. However, rice plants expressing ZmGF14-6 either in a constitutive or under a pathogen-inducible regime showed a higher susceptibility to infection by the fungal pathogens Fusarium verticillioides and Magnaporthe oryzae . Under infection conditions, a lower intensity in the expression of defence-related genes occurred in ZmGF14-6 rice plants. These findings support that ZmGF14-6 positively regulates drought tolerance in transgenic rice while negatively modulating the plant defence response to pathogen infection. Transient expression assays of fluorescently labelled ZmGF14-6 protein in onion epidermal cells revealed a widespread distribution of ZmGF14-6 in the cytoplasm and nucleus. Additionally, colocalization experiments of fluorescently labelled ZmGF14-6 with organelle markers, in combination with cell labelling with the endocytic tracer FM4-64, revealed a subcellular localization of ZmGF14-6 in the early endosomes. Taken together, these results improve our understanding of the role of ZmGF14-6 in stress signalling pathways, while indicating that ZmGF14-6 inversely regulates the plant response to biotic and abiotic stresses.
14-3-3 proteins are found in all eukaryotes where they act as regulators of diverse signalling pathways associated with a wide range of biological processes. In this study the functional characterization of the ZmGF14-6 gene encoding a maize 14-3-3 protein is reported. Gene expression analyses indicated that ZmGF14-6 is up-regulated by fungal infection and salt treatment in maize plants, whereas its expression is down-regulated by drought stress. It is reported that rice plants constitutively expressing ZmGF14-6 displayed enhanced tolerance to drought stress which was accompanied by a stronger induction of drought-associated rice genes. However, rice plants expressing ZmGF14-6 either in a constitutive or under a pathogen-inducible regime showed a higher susceptibility to infection by the fungal pathogens Fusarium verticillioides and Magnaporthe oryzae. Under infection conditions, a lower intensity in the expression of defence-related genes occurred in ZmGF14-6 rice plants. These findings support that ZmGF14-6 positively regulates drought tolerance in transgenic rice while negatively modulating the plant defence response to pathogen infection. Transient expression assays of fluorescently labelled ZmGF14-6 protein in onion epidermal cells revealed a widespread distribution of ZmGF14-6 in the cytoplasm and nucleus. Additionally, colocalization experiments of fluorescently labelled ZmGF14-6 with organelle markers, in combination with cell labelling with the endocytic tracer FM4-64, revealed a subcellular localization of ZmGF14-6 in the early endosomes. Taken together, these results improve our understanding of the role of ZmGF14-6 in stress signalling pathways, while indicating that ZmGF14-6 inversely regulates the plant response to biotic and abiotic stresses.
Author PENAS, Gisela
CAMPO, Sonia
MONTESINOS, Laura
PERIS-PERIS, Cristina
MESSEGUER, Joaquima
SAN SEGUNDO, Blanca
AuthorAffiliation 1 Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
2 Department of Plant Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
AuthorAffiliation_xml – name: 1 Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– name: 2 Department of Plant Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
Author_xml – sequence: 1
  givenname: Sonia
  surname: CAMPO
  fullname: CAMPO, Sonia
  organization: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– sequence: 2
  givenname: Cristina
  surname: PERIS-PERIS
  fullname: PERIS-PERIS, Cristina
  organization: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– sequence: 3
  givenname: Laura
  surname: MONTESINOS
  fullname: MONTESINOS, Laura
  organization: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– sequence: 4
  givenname: Gisela
  surname: PENAS
  fullname: PENAS, Gisela
  organization: Department of Plant Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– sequence: 5
  givenname: Joaquima
  surname: MESSEGUER
  fullname: MESSEGUER, Joaquima
  organization: Department of Plant Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
– sequence: 6
  givenname: Blanca
  surname: SAN SEGUNDO
  fullname: SAN SEGUNDO, Blanca
  organization: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Parc de Recerca UAB, Edifici CRAG, Campus UAB, Bellaterra (Cerdanyola del Vallés), 08193 Barcelona, Spain
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IsDoiOpenAccess true
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Issue 2
Keywords 14-3-3 proteins
early endosomes
Monocotyledones
Plant pathogen
Environmental factor
Water stress
Cereal crop
Abiotic factor
abiotic stress
Fungi
Promoter
Oryza sativa
Gene
Gramineae
Pathogenic
Angiospermae
Botany
Fungi Imperfecti
ZmPR4 promoter
Drought
Endosome
Biotic factor
Ascomycota
Zea mays
Magnaporthe oryzae
Tolerance
Protein
Infection
Fusarium verticillioides
biotic stress
Spermatophyta
Language English
License CC BY 4.0
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
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Present address: Institute of Food and Agricultural Technology-CeRTA-CIDSAV, University of Girona, Avda. Lluis Santaló, s/n 17071 Girona, Spain
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PublicationTitle Journal of experimental botany
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Snippet 14-3-3 proteins are found in all eukaryotes where they act as regulators of diverse signalling pathways associated with a wide range of biological processes....
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SubjectTerms 14-3-3 Proteins - genetics
14-3-3 Proteins - metabolism
Biological and medical sciences
Disease Susceptibility - immunology
Disease Susceptibility - microbiology
DNA, Complementary - genetics
Droughts
Fundamental and applied biological sciences. Psychology
Fungal plant pathogens
Fusarium - physiology
Gene Expression Regulation, Plant - physiology
Magnaporthe - physiology
Onions - genetics
Onions - metabolism
Oryza - genetics
Oryza - immunology
Oryza - microbiology
Oryza - physiology
Phytopathology. Animal pests. Plant and forest protection
Plant Diseases - immunology
Plant Diseases - microbiology
Plant physiology and development
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Roots - genetics
Plant Roots - immunology
Plant Roots - microbiology
Plant Roots - physiology
Plants, Genetically Modified
Promoter Regions, Genetic - genetics
Recombinant Proteins - isolation & purification
Research Papers
RNA, Plant - genetics
Seedlings - genetics
Seedlings - immunology
Seedlings - microbiology
Seedlings - physiology
Signal Transduction - physiology
Sodium Chloride - pharmacology
Stress, Physiological - physiology
Transcription Factors - genetics
Transcription Factors - metabolism
Up-Regulation
Zea mays - genetics
Title Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection
URI https://www.ncbi.nlm.nih.gov/pubmed/22016430
https://search.proquest.com/docview/915632372
https://pubmed.ncbi.nlm.nih.gov/PMC3254693
Volume 63
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