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Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm

BACKGROUND: Cell separation that occurs during fleshy fruit abscission and dry fruit dehiscence facilitates seed dispersal, the final stage of plant reproductive development. While our understanding of the evolutionary context of cell separation is limited mainly to the eudicot model systems tomato...

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Autores principales: Roongsattham, Peerapat, Morcillo, Fabienne, Jantasuriyarat, Chatchawan, Pizot, Maxime, Moussu, Steven, Jayaweera, Dasuni, Collin, Myriam, Gonzalez-Carranza, Zinnia H, Amblard, Philippe, Tregear, James W, Tragoonrung, Somvong, Verdeil, Jean-Luc, Tranbarger, Timothy J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3546427/
https://www.ncbi.nlm.nih.gov/pubmed/22920238
http://dx.doi.org/10.1186/1471-2229-12-150
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author Roongsattham, Peerapat
Morcillo, Fabienne
Jantasuriyarat, Chatchawan
Pizot, Maxime
Moussu, Steven
Jayaweera, Dasuni
Collin, Myriam
Gonzalez-Carranza, Zinnia H
Amblard, Philippe
Tregear, James W
Tragoonrung, Somvong
Verdeil, Jean-Luc
Tranbarger, Timothy J
author_facet Roongsattham, Peerapat
Morcillo, Fabienne
Jantasuriyarat, Chatchawan
Pizot, Maxime
Moussu, Steven
Jayaweera, Dasuni
Collin, Myriam
Gonzalez-Carranza, Zinnia H
Amblard, Philippe
Tregear, James W
Tragoonrung, Somvong
Verdeil, Jean-Luc
Tranbarger, Timothy J
author_sort Roongsattham, Peerapat
collection PubMed
description BACKGROUND: Cell separation that occurs during fleshy fruit abscission and dry fruit dehiscence facilitates seed dispersal, the final stage of plant reproductive development. While our understanding of the evolutionary context of cell separation is limited mainly to the eudicot model systems tomato and Arabidopsis, less is known about the mechanisms underlying fruit abscission in crop species, monocots in particular. The polygalacturonase (PG) multigene family encodes enzymes involved in the depolymerisation of pectin homogalacturonan within the primary cell wall and middle lamella. PG activity is commonly found in the separation layers during organ abscission and dehiscence, however, little is known about how this gene family has diverged since the separation of monocot and eudicots and the consequence of this divergence on the abscission process. RESULTS: The objective of the current study was to identify PGs responsible for the high activity previously observed in the abscission zone (AZ) during fruit shedding of the tropical monocot oil palm, and to analyze PG gene expression during oil palm fruit ripening and abscission. We identified 14 transcripts that encode PGs, all of which are expressed in the base of the oil palm fruit. The accumulation of five PG transcripts increase, four decrease and five do not change during ethylene treatments that induce cell separation. One PG transcript (EgPG4) is the most highly induced in the fruit base, with a 700–5000 fold increase during the ethylene treatment. In situ hybridization experiments indicate that the EgPG4 transcript increases preferentially in the AZ cell layers in the base of the fruit in response to ethylene prior to cell separation. CONCLUSIONS: The expression pattern of EgPG4 is consistent with the temporal and spatial requirements for cell separation to occur during oil palm fruit shedding. The sequence diversity of PGs and the complexity of their expression in the oil palm fruit tissues contrast with data from tomato, suggesting functional divergence underlying the ripening and abscission processes has occurred between these two fruit species. Furthermore, phylogenetic analysis of EgPG4 with PGs from other species suggests some conservation, but also diversification has occurred between monocots and eudicots, in particular between dry and fleshy fruit species.
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spelling pubmed-35464272013-01-17 Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm Roongsattham, Peerapat Morcillo, Fabienne Jantasuriyarat, Chatchawan Pizot, Maxime Moussu, Steven Jayaweera, Dasuni Collin, Myriam Gonzalez-Carranza, Zinnia H Amblard, Philippe Tregear, James W Tragoonrung, Somvong Verdeil, Jean-Luc Tranbarger, Timothy J BMC Plant Biol Research Article BACKGROUND: Cell separation that occurs during fleshy fruit abscission and dry fruit dehiscence facilitates seed dispersal, the final stage of plant reproductive development. While our understanding of the evolutionary context of cell separation is limited mainly to the eudicot model systems tomato and Arabidopsis, less is known about the mechanisms underlying fruit abscission in crop species, monocots in particular. The polygalacturonase (PG) multigene family encodes enzymes involved in the depolymerisation of pectin homogalacturonan within the primary cell wall and middle lamella. PG activity is commonly found in the separation layers during organ abscission and dehiscence, however, little is known about how this gene family has diverged since the separation of monocot and eudicots and the consequence of this divergence on the abscission process. RESULTS: The objective of the current study was to identify PGs responsible for the high activity previously observed in the abscission zone (AZ) during fruit shedding of the tropical monocot oil palm, and to analyze PG gene expression during oil palm fruit ripening and abscission. We identified 14 transcripts that encode PGs, all of which are expressed in the base of the oil palm fruit. The accumulation of five PG transcripts increase, four decrease and five do not change during ethylene treatments that induce cell separation. One PG transcript (EgPG4) is the most highly induced in the fruit base, with a 700–5000 fold increase during the ethylene treatment. In situ hybridization experiments indicate that the EgPG4 transcript increases preferentially in the AZ cell layers in the base of the fruit in response to ethylene prior to cell separation. CONCLUSIONS: The expression pattern of EgPG4 is consistent with the temporal and spatial requirements for cell separation to occur during oil palm fruit shedding. The sequence diversity of PGs and the complexity of their expression in the oil palm fruit tissues contrast with data from tomato, suggesting functional divergence underlying the ripening and abscission processes has occurred between these two fruit species. Furthermore, phylogenetic analysis of EgPG4 with PGs from other species suggests some conservation, but also diversification has occurred between monocots and eudicots, in particular between dry and fleshy fruit species. BioMed Central 2012-08-25 /pmc/articles/PMC3546427/ /pubmed/22920238 http://dx.doi.org/10.1186/1471-2229-12-150 Text en Copyright ©2012 Roongsattham et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Roongsattham, Peerapat
Morcillo, Fabienne
Jantasuriyarat, Chatchawan
Pizot, Maxime
Moussu, Steven
Jayaweera, Dasuni
Collin, Myriam
Gonzalez-Carranza, Zinnia H
Amblard, Philippe
Tregear, James W
Tragoonrung, Somvong
Verdeil, Jean-Luc
Tranbarger, Timothy J
Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title_full Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title_fullStr Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title_full_unstemmed Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title_short Temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
title_sort temporal and spatial expression of polygalacturonase gene family members reveals divergent regulation during fleshy fruit ripening and abscission in the monocot species oil palm
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3546427/
https://www.ncbi.nlm.nih.gov/pubmed/22920238
http://dx.doi.org/10.1186/1471-2229-12-150
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