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Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission

BACKGROUND: Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ). To determine the mechanisms of fleshy fruit abscission of the monocot oil palm (Elaeis guineensis Jacq.) compared with other abscission systems, we performed mu...

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Autores principales: Fooyontphanich, Kim, Morcillo, Fabienne, Joët, Thierry, Dussert, Stéphane, Serret, Julien, Collin, Myriam, Amblard, Philippe, Tangphatsornruang, Sithichoke, Roongsattham, Peerapat, Jantasuriyarat, Chatchawan, Verdeil, Jean-Luc, Tranbarger, Timothy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7879690/
https://www.ncbi.nlm.nih.gov/pubmed/33573592
http://dx.doi.org/10.1186/s12870-021-02874-1
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author Fooyontphanich, Kim
Morcillo, Fabienne
Joët, Thierry
Dussert, Stéphane
Serret, Julien
Collin, Myriam
Amblard, Philippe
Tangphatsornruang, Sithichoke
Roongsattham, Peerapat
Jantasuriyarat, Chatchawan
Verdeil, Jean-Luc
Tranbarger, Timothy J.
author_facet Fooyontphanich, Kim
Morcillo, Fabienne
Joët, Thierry
Dussert, Stéphane
Serret, Julien
Collin, Myriam
Amblard, Philippe
Tangphatsornruang, Sithichoke
Roongsattham, Peerapat
Jantasuriyarat, Chatchawan
Verdeil, Jean-Luc
Tranbarger, Timothy J.
author_sort Fooyontphanich, Kim
collection PubMed
description BACKGROUND: Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ). To determine the mechanisms of fleshy fruit abscission of the monocot oil palm (Elaeis guineensis Jacq.) compared with other abscission systems, we performed multi-scale comparative transcriptome analyses on fruit targeting the developing primary AZ and adjacent tissues. RESULTS: Combining between-tissue developmental comparisons with exogenous ethylene treatments, and naturally occurring abscission in the field, RNAseq analysis revealed a robust core set of 168 genes with differentially regulated expression, spatially associated with the ripe fruit AZ, and temporally restricted to the abscission timing. The expression of a set of candidate genes was validated by qRT-PCR in the fruit AZ of a natural oil palm variant with blocked fruit abscission, which provides evidence for their functions during abscission. Our results substantiate the conservation of gene function between dicot dry fruit dehiscence and monocot fleshy fruit abscission. The study also revealed major metabolic transitions occur in the AZ during abscission, including key senescence marker genes and transcriptional regulators, in addition to genes involved in nutrient recycling and reallocation, alternative routes for energy supply and adaptation to oxidative stress. CONCLUSIONS: The study provides the first reference transcriptome of a monocot fleshy fruit abscission zone and provides insight into the mechanisms underlying abscission by identifying key genes with functional roles and processes, including metabolic transitions, cell wall modifications, signalling, stress adaptations and transcriptional regulation, that occur during ripe fruit abscission of the monocot oil palm. The transcriptome data comprises an original reference and resource useful towards understanding the evolutionary basis of this fundamental plant process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02874-1.
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spelling pubmed-78796902021-02-17 Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission Fooyontphanich, Kim Morcillo, Fabienne Joët, Thierry Dussert, Stéphane Serret, Julien Collin, Myriam Amblard, Philippe Tangphatsornruang, Sithichoke Roongsattham, Peerapat Jantasuriyarat, Chatchawan Verdeil, Jean-Luc Tranbarger, Timothy J. BMC Plant Biol Original Research BACKGROUND: Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ). To determine the mechanisms of fleshy fruit abscission of the monocot oil palm (Elaeis guineensis Jacq.) compared with other abscission systems, we performed multi-scale comparative transcriptome analyses on fruit targeting the developing primary AZ and adjacent tissues. RESULTS: Combining between-tissue developmental comparisons with exogenous ethylene treatments, and naturally occurring abscission in the field, RNAseq analysis revealed a robust core set of 168 genes with differentially regulated expression, spatially associated with the ripe fruit AZ, and temporally restricted to the abscission timing. The expression of a set of candidate genes was validated by qRT-PCR in the fruit AZ of a natural oil palm variant with blocked fruit abscission, which provides evidence for their functions during abscission. Our results substantiate the conservation of gene function between dicot dry fruit dehiscence and monocot fleshy fruit abscission. The study also revealed major metabolic transitions occur in the AZ during abscission, including key senescence marker genes and transcriptional regulators, in addition to genes involved in nutrient recycling and reallocation, alternative routes for energy supply and adaptation to oxidative stress. CONCLUSIONS: The study provides the first reference transcriptome of a monocot fleshy fruit abscission zone and provides insight into the mechanisms underlying abscission by identifying key genes with functional roles and processes, including metabolic transitions, cell wall modifications, signalling, stress adaptations and transcriptional regulation, that occur during ripe fruit abscission of the monocot oil palm. The transcriptome data comprises an original reference and resource useful towards understanding the evolutionary basis of this fundamental plant process. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02874-1. BioMed Central 2021-02-11 /pmc/articles/PMC7879690/ /pubmed/33573592 http://dx.doi.org/10.1186/s12870-021-02874-1 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Original Research
Fooyontphanich, Kim
Morcillo, Fabienne
Joët, Thierry
Dussert, Stéphane
Serret, Julien
Collin, Myriam
Amblard, Philippe
Tangphatsornruang, Sithichoke
Roongsattham, Peerapat
Jantasuriyarat, Chatchawan
Verdeil, Jean-Luc
Tranbarger, Timothy J.
Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title_full Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title_fullStr Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title_full_unstemmed Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title_short Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
title_sort multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7879690/
https://www.ncbi.nlm.nih.gov/pubmed/33573592
http://dx.doi.org/10.1186/s12870-021-02874-1
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