AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening

The involvement of ethylene in fruit ripening is well documented, though knowledge regarding the crosstalk between ethylene and other hormones in ripening is lacking. We discovered that AUXIN RESPONSE FACTOR 2A (ARF2A), a recognized auxin signaling component, functions in the control of ripening. AR...

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Main Authors: Breitel, Dario A., Chappell-Maor, Louise, Meir, Sagit, Panizel, Irina, Puig, Clara Pons, Hao, Yanwei, Yifhar, Tamar, Yasuor, Hagai, Zouine, Mohamed, Bouzayen, Mondher, Granell Richart, Antonio, Rogachev, Ilana, Aharoni, Asaph
Format: Online
Language:English
Published: Public Library of Science 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4784954/
id pubmed-4784954
recordtype oai_dc
spelling pubmed-47849542016-03-23 AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening Breitel, Dario A. Chappell-Maor, Louise Meir, Sagit Panizel, Irina Puig, Clara Pons Hao, Yanwei Yifhar, Tamar Yasuor, Hagai Zouine, Mohamed Bouzayen, Mondher Granell Richart, Antonio Rogachev, Ilana Aharoni, Asaph Research Article The involvement of ethylene in fruit ripening is well documented, though knowledge regarding the crosstalk between ethylene and other hormones in ripening is lacking. We discovered that AUXIN RESPONSE FACTOR 2A (ARF2A), a recognized auxin signaling component, functions in the control of ripening. ARF2A expression is ripening regulated and reduced in the rin, nor and nr ripening mutants. It is also responsive to exogenous application of ethylene, auxin and abscisic acid (ABA). Over-expressing ARF2A in tomato resulted in blotchy ripening in which certain fruit regions turn red and possess accelerated ripening. ARF2A over-expressing fruit displayed early ethylene emission and ethylene signaling inhibition delayed their ripening phenotype, suggesting ethylene dependency. Both green and red fruit regions showed the induction of ethylene signaling components and master regulators of ripening. Comprehensive hormone profiling revealed that altered ARF2A expression in fruit significantly modified abscisates, cytokinins and salicylic acid while gibberellic acid and auxin metabolites were unaffected. Silencing of ARF2A further validated these observations as reducing ARF2A expression let to retarded fruit ripening, parthenocarpy and a disturbed hormonal profile. Finally, we show that ARF2A both homodimerizes and interacts with the ABA STRESS RIPENING (ASR1) protein, suggesting that ASR1 might be linking ABA and ethylene-dependent ripening. These results revealed that ARF2A interconnects signals of ethylene and additional hormones to co-ordinate the capacity of fruit tissue to initiate the complex ripening process. Public Library of Science 2016-03-09 /pmc/articles/PMC4784954/ /pubmed/26959229 http://dx.doi.org/10.1371/journal.pgen.1005903 Text en © 2016 Breitel et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Breitel, Dario A.
Chappell-Maor, Louise
Meir, Sagit
Panizel, Irina
Puig, Clara Pons
Hao, Yanwei
Yifhar, Tamar
Yasuor, Hagai
Zouine, Mohamed
Bouzayen, Mondher
Granell Richart, Antonio
Rogachev, Ilana
Aharoni, Asaph
spellingShingle Breitel, Dario A.
Chappell-Maor, Louise
Meir, Sagit
Panizel, Irina
Puig, Clara Pons
Hao, Yanwei
Yifhar, Tamar
Yasuor, Hagai
Zouine, Mohamed
Bouzayen, Mondher
Granell Richart, Antonio
Rogachev, Ilana
Aharoni, Asaph
AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
author_facet Breitel, Dario A.
Chappell-Maor, Louise
Meir, Sagit
Panizel, Irina
Puig, Clara Pons
Hao, Yanwei
Yifhar, Tamar
Yasuor, Hagai
Zouine, Mohamed
Bouzayen, Mondher
Granell Richart, Antonio
Rogachev, Ilana
Aharoni, Asaph
author_sort Breitel, Dario A.
title AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
title_short AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
title_full AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
title_fullStr AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
title_full_unstemmed AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening
title_sort auxin response factor 2 intersects hormonal signals in the regulation of tomato fruit ripening
description The involvement of ethylene in fruit ripening is well documented, though knowledge regarding the crosstalk between ethylene and other hormones in ripening is lacking. We discovered that AUXIN RESPONSE FACTOR 2A (ARF2A), a recognized auxin signaling component, functions in the control of ripening. ARF2A expression is ripening regulated and reduced in the rin, nor and nr ripening mutants. It is also responsive to exogenous application of ethylene, auxin and abscisic acid (ABA). Over-expressing ARF2A in tomato resulted in blotchy ripening in which certain fruit regions turn red and possess accelerated ripening. ARF2A over-expressing fruit displayed early ethylene emission and ethylene signaling inhibition delayed their ripening phenotype, suggesting ethylene dependency. Both green and red fruit regions showed the induction of ethylene signaling components and master regulators of ripening. Comprehensive hormone profiling revealed that altered ARF2A expression in fruit significantly modified abscisates, cytokinins and salicylic acid while gibberellic acid and auxin metabolites were unaffected. Silencing of ARF2A further validated these observations as reducing ARF2A expression let to retarded fruit ripening, parthenocarpy and a disturbed hormonal profile. Finally, we show that ARF2A both homodimerizes and interacts with the ABA STRESS RIPENING (ASR1) protein, suggesting that ASR1 might be linking ABA and ethylene-dependent ripening. These results revealed that ARF2A interconnects signals of ethylene and additional hormones to co-ordinate the capacity of fruit tissue to initiate the complex ripening process.
publisher Public Library of Science
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4784954/
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