Molecular study of drought response in the Mediterranean conifer Pinus pinaster Ait.: Differential transcriptomic profiling reveals constitutive water deficit‐independent drought tolerance mechanisms

Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of soft...

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Published inEcology and evolution Vol. 10; no. 18; pp. 9788 - 9807
Main Authors de María, Nuria, Guevara, María Ángeles, Perdiguero, Pedro, Vélez, María Dolores, Cabezas, José Antonio, López‐Hinojosa, Miriam, Li, Zhen, Díaz, Luís Manuel, Pizarro, Alberto, Mancha, José Antonio, Sterck, Lieven, Sánchez‐Gómez, David, Miguel, Célia, Collada, Carmen, Díaz‐Sala, María Carmen, Cervera, María Teresa
Format Journal Article
LanguageEnglish
Published Bognor Regis John Wiley & Sons, Inc 01.09.2020
John Wiley and Sons Inc
Wiley
Subjects
Online AccessGet full text
ISSN2045-7758
2045-7758
DOI10.1002/ece3.6613

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Abstract Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought. The manuscript presents the transcriptome of maritime pine trees that show contrasted response to drought. Comparison of transcriptomic profiles at the organ level allowed to identify organ‐specific and genotype‐specific transcripts as well as differentially expressed genes between organs, genotypes, and treatments. The results also point out to different response strategies, with tolerant plants pre‐adapted for coping with drought by expressing constitutively stress‐related genes that only can be detected in sensitive plants submitted to drought.
AbstractList Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought.
Adaptation of long-living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full-sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well-watered and moderate water stress. The comparative analyses led us to identify organ-specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought-sensitive and drought-tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre-adapted for coping with drought by constitutively expressing stress-related genes that are detected only in latter stages on sensitive individuals subjected to drought.Adaptation of long-living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full-sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well-watered and moderate water stress. The comparative analyses led us to identify organ-specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought-sensitive and drought-tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre-adapted for coping with drought by constitutively expressing stress-related genes that are detected only in latter stages on sensitive individuals subjected to drought.
Abstract Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought.
Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought. The manuscript presents the transcriptome of maritime pine trees that show contrasted response to drought. Comparison of transcriptomic profiles at the organ level allowed to identify organ‐specific and genotype‐specific transcripts as well as differentially expressed genes between organs, genotypes, and treatments. The results also point out to different response strategies, with tolerant plants pre‐adapted for coping with drought by expressing constitutively stress‐related genes that only can be detected in sensitive plants submitted to drought.
Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine ( Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought.
Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is one of the most significant stress factors determining tree growth and survival. Maritime pine (Pinus pinaster Ait.), the main source of softwood in southwestern Europe, is subjected to recurrent drought periods which, according to climate change predictions for the years to come, will progressively increase in the Mediterranean region. The mechanisms regulating pine adaptive responses to environment are still largely unknown. The aim of this work was to go a step further in understanding the molecular mechanisms underlying maritime pine response to water stress and drought tolerance at the whole plant level. A global transcriptomic profiling of roots, stems, and needles was conducted to analyze the performance of siblings showing contrasted responses to water deficit from an ad hoc designed full‐sib family. Although P. pinaster is considered a recalcitrant species for vegetative propagation in adult phase, the analysis was conducted using vegetatively propagated trees exposed to two treatments: well‐watered and moderate water stress. The comparative analyses led us to identify organ‐specific genes, constitutively expressed as well as differentially expressed when comparing control versus water stress conditions, in drought‐sensitive and drought‐tolerant genotypes. Different response strategies can point out, with tolerant individuals being pre‐adapted for coping with drought by constitutively expressing stress‐related genes that are detected only in latter stages on sensitive individuals subjected to drought. The manuscript presents the transcriptome of maritime pine trees that show contrasted response to drought. Comparison of transcriptomic profiles at the organ level allowed to identify organ‐specific and genotype‐specific transcripts as well as differentially expressed genes between organs, genotypes, and treatments. The results also point out to different response strategies, with tolerant plants pre‐adapted for coping with drought by expressing constitutively stress‐related genes that only can be detected in sensitive plants submitted to drought.
Author de María, Nuria
Li, Zhen
Sánchez‐Gómez, David
Pizarro, Alberto
López‐Hinojosa, Miriam
Vélez, María Dolores
Mancha, José Antonio
Cervera, María Teresa
Perdiguero, Pedro
Díaz‐Sala, María Carmen
Sterck, Lieven
Collada, Carmen
Guevara, María Ángeles
Díaz, Luís Manuel
Miguel, Célia
Cabezas, José Antonio
AuthorAffiliation 10 Instituto de Biologia Experimental e Tecnológica (iBET) Oeiras Portugal
6 VIB‐UGent Center for Plant Systems Biology Ghent Belgium
11 Grupo de investigación Sistemas Naturales e Historia Forestal UPM Madrid Spain
4 Departamento de Cultivos Herbáceos Centro de Investigación Agroforestal de Albaladejito Cuenca Spain
7 Bioinformatics Institute Ghent Ghent University Ghent Belgium
3 Centro de Investigación en Sanidad Animal (CISA‐INIA) Madrid Spain
5 Ghent University Department of Plant Biotechnology and Bioinformatics Ghent Belgium
8 Departamento de Ciencias de la Vida Universidad de Alcalá Alcalá de Henares Spain
2 Unidad Mixta de Genómica y Ecofisiología Forestal Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) Madrid Spain
1 Departamento de Ecología y Genética Forestal Centro de Investigación Forestal (CIFOR) Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) Madrid Spain
9 BioISI‐Biosystems & Inte
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ContentType Journal Article
Copyright 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd
2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
Copyright_xml – notice: 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd
– notice: 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
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– ident: e_1_2_10_77_1
  doi: 10.3389/fpls.2014.00086
– ident: e_1_2_10_58_1
  doi: 10.1007/s11105-014-0705-5
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Snippet Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is...
Adaptation of long-living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water deficit is...
Abstract Adaptation of long‐living forest trees to respond to environmental changes is essential to secure their performance under adverse conditions. Water...
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StartPage 9788
SubjectTerms Biosynthesis
Climate change
Climate prediction
Comparative analysis
Design
differential transcript profiles
Drought resistance
Efficiency
Environmental changes
Genes
Genomes
Genotype & phenotype
Genotypes
Homeostasis
Kinases
Mediterranean conifer
Molecular modelling
Original Research
Physiology
Pine
Pine needles
Pine trees
Pinus pinaster
Plant propagation
pre‐adapted genotypes
Propagation
response strategies
Softwoods
Stress propagation
Trees
Water deficit
Water stress
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Title Molecular study of drought response in the Mediterranean conifer Pinus pinaster Ait.: Differential transcriptomic profiling reveals constitutive water deficit‐independent drought tolerance mechanisms
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