Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica

Background: Somatic embryogenesis (SE) is one of the most promising processes for large-scale dissemination of elite varieties. However, for many plant species, optimizing SE protocols still relies on a trial and error approach. We report the first global scale transcriptome profiling performed at all developmental stages of SE in coffee to unravel the mechanisms that regulate cell fate and totipotency. Results: RNA-seq of 48 samples (12 developmental stages × 4 biological replicates) generated 90 million high quality reads per sample, approximately 74% of which were uniquely mapped to the Arabica genome. First, the statistical analysis of transcript data clearly grouped SE developmental stages into seven important phases (Leaf, Dedifferentiation, Primary callus, Embryogenic callus, Embryogenic cell clusters, Redifferentiation and Embryo) enabling the identification of six key developmental phase switches, which are strategic for the overall biological efficiency of embryo regeneration. Differential gene expression and functional analysis showed that genes encoding transcription factors, stress-related genes, metabolism-related genes and hormone signaling-related genes were significantly enriched. Second, the standard environmental drivers used to control SE, i.e. light, growth regulators and cell density, were clearly perceived at the molecular level at different developmental stages. Third, expression profiles of auxin-related genes, transcription factor-related genes and secondary metabolism-related genes were analyzed during SE. Gene co-expression networks were also inferred. Auxin-related genes were upregulated during dedifferentiation and redifferentiation while transcription factor-related genes were switched on from the embryogenic callus and onward. Secondary metabolism-related genes were switched off during dedifferentiation and switched back on at the onset of redifferentiation. Secondary metabolites and endogenous IAA content were tightly linked with their respective gene expression. Lastly, comparing Arabica embryogenic and non-embryogenic cell transcriptomes enabled the identification of biological processes involved in the acquisition of embryogenic capacity. Conclusions: The present analysis showed that transcript fingerprints are discriminating signatures of cell fate and are under the direct influence of environmental drivers. A total of 23 molecular candidates were successfully identified overall the 12 developmental stages and can be tested in many plant species to optimize SE protocols in a rational way.

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Main Authors: Awada, Rayan, Lepelley, Maud, Breton, David, Charpagne, Aline, Campa, Claudine, Berry, Victoria, Georget, Frederic, Breitler, Jean-Christophe, Leran, Sophie, Djerrab, Doaa, Martinez-Seidel, Federico, Descombes, Patrick, Crouzillat, Dominique, Bertrand, Benoît, Etienne, Hervé
Format: article biblioteca
Language:eng
Subjects:F30 - Génétique et amélioration des plantes, Embryogénèse somatique, marqueur génétique, génomique, Coffea arabica, transcriptome, http://aims.fao.org/aos/agrovoc/c_36911, http://aims.fao.org/aos/agrovoc/c_24030, http://aims.fao.org/aos/agrovoc/c_92382, http://aims.fao.org/aos/agrovoc/c_1721, http://aims.fao.org/aos/agrovoc/c_620c5378,
Online Access:http://agritrop.cirad.fr/603581/
http://agritrop.cirad.fr/603581/1/R%20Awada%20et%20al.%202023.pdf
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record_format koha
institution CIRAD FR
collection DSpace
country Francia
countrycode FR
component Bibliográfico
access En linea
databasecode dig-cirad-fr
tag biblioteca
region Europa del Oeste
libraryname Biblioteca del CIRAD Francia
language eng
topic F30 - Génétique et amélioration des plantes
Embryogénèse somatique
marqueur génétique
génomique
Coffea arabica
transcriptome
http://aims.fao.org/aos/agrovoc/c_36911
http://aims.fao.org/aos/agrovoc/c_24030
http://aims.fao.org/aos/agrovoc/c_92382
http://aims.fao.org/aos/agrovoc/c_1721
http://aims.fao.org/aos/agrovoc/c_620c5378
F30 - Génétique et amélioration des plantes
Embryogénèse somatique
marqueur génétique
génomique
Coffea arabica
transcriptome
http://aims.fao.org/aos/agrovoc/c_36911
http://aims.fao.org/aos/agrovoc/c_24030
http://aims.fao.org/aos/agrovoc/c_92382
http://aims.fao.org/aos/agrovoc/c_1721
http://aims.fao.org/aos/agrovoc/c_620c5378
spellingShingle F30 - Génétique et amélioration des plantes
Embryogénèse somatique
marqueur génétique
génomique
Coffea arabica
transcriptome
http://aims.fao.org/aos/agrovoc/c_36911
http://aims.fao.org/aos/agrovoc/c_24030
http://aims.fao.org/aos/agrovoc/c_92382
http://aims.fao.org/aos/agrovoc/c_1721
http://aims.fao.org/aos/agrovoc/c_620c5378
F30 - Génétique et amélioration des plantes
Embryogénèse somatique
marqueur génétique
génomique
Coffea arabica
transcriptome
http://aims.fao.org/aos/agrovoc/c_36911
http://aims.fao.org/aos/agrovoc/c_24030
http://aims.fao.org/aos/agrovoc/c_92382
http://aims.fao.org/aos/agrovoc/c_1721
http://aims.fao.org/aos/agrovoc/c_620c5378
Awada, Rayan
Lepelley, Maud
Breton, David
Charpagne, Aline
Campa, Claudine
Berry, Victoria
Georget, Frederic
Breitler, Jean-Christophe
Leran, Sophie
Djerrab, Doaa
Martinez-Seidel, Federico
Descombes, Patrick
Crouzillat, Dominique
Bertrand, Benoît
Etienne, Hervé
Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
description Background: Somatic embryogenesis (SE) is one of the most promising processes for large-scale dissemination of elite varieties. However, for many plant species, optimizing SE protocols still relies on a trial and error approach. We report the first global scale transcriptome profiling performed at all developmental stages of SE in coffee to unravel the mechanisms that regulate cell fate and totipotency. Results: RNA-seq of 48 samples (12 developmental stages × 4 biological replicates) generated 90 million high quality reads per sample, approximately 74% of which were uniquely mapped to the Arabica genome. First, the statistical analysis of transcript data clearly grouped SE developmental stages into seven important phases (Leaf, Dedifferentiation, Primary callus, Embryogenic callus, Embryogenic cell clusters, Redifferentiation and Embryo) enabling the identification of six key developmental phase switches, which are strategic for the overall biological efficiency of embryo regeneration. Differential gene expression and functional analysis showed that genes encoding transcription factors, stress-related genes, metabolism-related genes and hormone signaling-related genes were significantly enriched. Second, the standard environmental drivers used to control SE, i.e. light, growth regulators and cell density, were clearly perceived at the molecular level at different developmental stages. Third, expression profiles of auxin-related genes, transcription factor-related genes and secondary metabolism-related genes were analyzed during SE. Gene co-expression networks were also inferred. Auxin-related genes were upregulated during dedifferentiation and redifferentiation while transcription factor-related genes were switched on from the embryogenic callus and onward. Secondary metabolism-related genes were switched off during dedifferentiation and switched back on at the onset of redifferentiation. Secondary metabolites and endogenous IAA content were tightly linked with their respective gene expression. Lastly, comparing Arabica embryogenic and non-embryogenic cell transcriptomes enabled the identification of biological processes involved in the acquisition of embryogenic capacity. Conclusions: The present analysis showed that transcript fingerprints are discriminating signatures of cell fate and are under the direct influence of environmental drivers. A total of 23 molecular candidates were successfully identified overall the 12 developmental stages and can be tested in many plant species to optimize SE protocols in a rational way.
format article
topic_facet F30 - Génétique et amélioration des plantes
Embryogénèse somatique
marqueur génétique
génomique
Coffea arabica
transcriptome
http://aims.fao.org/aos/agrovoc/c_36911
http://aims.fao.org/aos/agrovoc/c_24030
http://aims.fao.org/aos/agrovoc/c_92382
http://aims.fao.org/aos/agrovoc/c_1721
http://aims.fao.org/aos/agrovoc/c_620c5378
author Awada, Rayan
Lepelley, Maud
Breton, David
Charpagne, Aline
Campa, Claudine
Berry, Victoria
Georget, Frederic
Breitler, Jean-Christophe
Leran, Sophie
Djerrab, Doaa
Martinez-Seidel, Federico
Descombes, Patrick
Crouzillat, Dominique
Bertrand, Benoît
Etienne, Hervé
author_facet Awada, Rayan
Lepelley, Maud
Breton, David
Charpagne, Aline
Campa, Claudine
Berry, Victoria
Georget, Frederic
Breitler, Jean-Christophe
Leran, Sophie
Djerrab, Doaa
Martinez-Seidel, Federico
Descombes, Patrick
Crouzillat, Dominique
Bertrand, Benoît
Etienne, Hervé
author_sort Awada, Rayan
title Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
title_short Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
title_full Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
title_fullStr Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
title_full_unstemmed Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica
title_sort global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in coffea arabica
url http://agritrop.cirad.fr/603581/
http://agritrop.cirad.fr/603581/1/R%20Awada%20et%20al.%202023.pdf
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spelling dig-cirad-fr-6035812024-01-29T04:29:35Z http://agritrop.cirad.fr/603581/ http://agritrop.cirad.fr/603581/ Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica. Awada Rayan, Lepelley Maud, Breton David, Charpagne Aline, Campa Claudine, Berry Victoria, Georget Frederic, Breitler Jean-Christophe, Leran Sophie, Djerrab Doaa, Martinez-Seidel Federico, Descombes Patrick, Crouzillat Dominique, Bertrand Benoît, Etienne Hervé. 2023. BMC Genomics, 24:41, 19 p.https://doi.org/10.1186/s12864-022-09098-z <https://doi.org/10.1186/s12864-022-09098-z> Global transcriptome profiling reveals differential regulatory, metabolic and hormonal networks during somatic embryogenesis in Coffea arabica Awada, Rayan Lepelley, Maud Breton, David Charpagne, Aline Campa, Claudine Berry, Victoria Georget, Frederic Breitler, Jean-Christophe Leran, Sophie Djerrab, Doaa Martinez-Seidel, Federico Descombes, Patrick Crouzillat, Dominique Bertrand, Benoît Etienne, Hervé eng 2023 BMC Genomics F30 - Génétique et amélioration des plantes Embryogénèse somatique marqueur génétique génomique Coffea arabica transcriptome http://aims.fao.org/aos/agrovoc/c_36911 http://aims.fao.org/aos/agrovoc/c_24030 http://aims.fao.org/aos/agrovoc/c_92382 http://aims.fao.org/aos/agrovoc/c_1721 http://aims.fao.org/aos/agrovoc/c_620c5378 Background: Somatic embryogenesis (SE) is one of the most promising processes for large-scale dissemination of elite varieties. However, for many plant species, optimizing SE protocols still relies on a trial and error approach. We report the first global scale transcriptome profiling performed at all developmental stages of SE in coffee to unravel the mechanisms that regulate cell fate and totipotency. Results: RNA-seq of 48 samples (12 developmental stages × 4 biological replicates) generated 90 million high quality reads per sample, approximately 74% of which were uniquely mapped to the Arabica genome. First, the statistical analysis of transcript data clearly grouped SE developmental stages into seven important phases (Leaf, Dedifferentiation, Primary callus, Embryogenic callus, Embryogenic cell clusters, Redifferentiation and Embryo) enabling the identification of six key developmental phase switches, which are strategic for the overall biological efficiency of embryo regeneration. Differential gene expression and functional analysis showed that genes encoding transcription factors, stress-related genes, metabolism-related genes and hormone signaling-related genes were significantly enriched. Second, the standard environmental drivers used to control SE, i.e. light, growth regulators and cell density, were clearly perceived at the molecular level at different developmental stages. Third, expression profiles of auxin-related genes, transcription factor-related genes and secondary metabolism-related genes were analyzed during SE. Gene co-expression networks were also inferred. Auxin-related genes were upregulated during dedifferentiation and redifferentiation while transcription factor-related genes were switched on from the embryogenic callus and onward. Secondary metabolism-related genes were switched off during dedifferentiation and switched back on at the onset of redifferentiation. Secondary metabolites and endogenous IAA content were tightly linked with their respective gene expression. Lastly, comparing Arabica embryogenic and non-embryogenic cell transcriptomes enabled the identification of biological processes involved in the acquisition of embryogenic capacity. Conclusions: The present analysis showed that transcript fingerprints are discriminating signatures of cell fate and are under the direct influence of environmental drivers. A total of 23 molecular candidates were successfully identified overall the 12 developmental stages and can be tested in many plant species to optimize SE protocols in a rational way. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/603581/1/R%20Awada%20et%20al.%202023.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1186/s12864-022-09098-z 10.1186/s12864-022-09098-z info:eu-repo/semantics/altIdentifier/doi/10.1186/s12864-022-09098-z info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1186/s12864-022-09098-z