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 in | Ecology and evolution Vol. 10; no. 18; pp. 9788 - 9807 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Bognor Regis
John Wiley & Sons, Inc
01.09.2020
John Wiley and Sons Inc Wiley |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2045-7758 2045-7758 |
| DOI | 10.1002/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. |
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| 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 |
| AuthorAffiliation_xml | – name: 5 Ghent University Department of Plant Biotechnology and Bioinformatics Ghent Belgium – name: 1 Departamento de Ecología y Genética Forestal Centro de Investigación Forestal (CIFOR) Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) Madrid Spain – name: 4 Departamento de Cultivos Herbáceos Centro de Investigación Agroforestal de Albaladejito Cuenca Spain – name: 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 – name: 6 VIB‐UGent Center for Plant Systems Biology Ghent Belgium – name: 7 Bioinformatics Institute Ghent Ghent University Ghent Belgium – name: 11 Grupo de investigación Sistemas Naturales e Historia Forestal UPM Madrid Spain – name: 8 Departamento de Ciencias de la Vida Universidad de Alcalá Alcalá de Henares Spain – name: 9 BioISI‐Biosystems & Integrative Sciences Institute Faculdade de Ciências Universidade de Lisboa Lisboa Portugal – name: 3 Centro de Investigación en Sanidad Animal (CISA‐INIA) Madrid Spain – name: 10 Instituto de Biologia Experimental e Tecnológica (iBET) Oeiras Portugal |
| Author_xml | – sequence: 1 givenname: Nuria orcidid: 0000-0003-4506-3980 surname: de María fullname: de María, Nuria organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 2 givenname: María Ángeles orcidid: 0000-0001-7399-3136 surname: Guevara fullname: Guevara, María Ángeles organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 3 givenname: Pedro orcidid: 0000-0002-5471-9550 surname: Perdiguero fullname: Perdiguero, Pedro organization: Centro de Investigación Agroforestal de Albaladejito – sequence: 4 givenname: María Dolores orcidid: 0000-0001-8871-5737 surname: Vélez fullname: Vélez, María Dolores organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 5 givenname: José Antonio orcidid: 0000-0002-4728-6072 surname: Cabezas fullname: Cabezas, José Antonio organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 6 givenname: Miriam orcidid: 0000-0002-7495-1517 surname: López‐Hinojosa fullname: López‐Hinojosa, Miriam organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 7 givenname: Zhen orcidid: 0000-0001-8920-9270 surname: Li fullname: Li, Zhen organization: Ghent University – sequence: 8 givenname: Luís Manuel surname: Díaz fullname: Díaz, Luís Manuel organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) – sequence: 9 givenname: Alberto surname: Pizarro fullname: Pizarro, Alberto organization: Universidad de Alcalá – sequence: 10 givenname: José Antonio surname: Mancha fullname: Mancha, José Antonio organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) – sequence: 11 givenname: Lieven orcidid: 0000-0001-7116-4000 surname: Sterck fullname: Sterck, Lieven organization: Ghent University – sequence: 12 givenname: David orcidid: 0000-0002-0588-9713 surname: Sánchez‐Gómez fullname: Sánchez‐Gómez, David organization: Centro de Investigación Agroforestal de Albaladejito – sequence: 13 givenname: Célia orcidid: 0000-0002-1427-952X surname: Miguel fullname: Miguel, Célia organization: Instituto de Biologia Experimental e Tecnológica (iBET) – sequence: 14 givenname: Carmen orcidid: 0000-0003-0236-1312 surname: Collada fullname: Collada, Carmen organization: UPM – sequence: 15 givenname: María Carmen orcidid: 0000-0001-6249-7540 surname: Díaz‐Sala fullname: Díaz‐Sala, María Carmen organization: Universidad de Alcalá – sequence: 16 givenname: María Teresa orcidid: 0000-0001-6797-2347 surname: Cervera fullname: Cervera, María Teresa email: cervera@inia.es organization: Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)/Universidad Politécnica de Madrid (UPM) |
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| 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. |
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| Language | English |
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| Notes | Nuria de María and M. Ángeles Guevara have contributed equally to this work. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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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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| 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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