Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis

Detalhes bibliográficos
Autor(a) principal: Cruz, Aline Bertinatto
Data de Publicação: 2017
Tipo de documento: Tese
Idioma: eng
Título da fonte: Biblioteca Digital de Teses e Dissertações da USP
Texto Completo: http://www.teses.usp.br/teses/disponiveis/41/41132/tde-05092017-104106/
Resumo: Fruit ripening is a highly coordinated process involving numerous structural, biochemical and physiological changes, many of which are influenced by both endogenous and environmental stimuli. Light signaling and plant hormones such as ethylene and auxins have been identified as important regulators of tomato fruit ripening. However, it is still not fully understood how light and hormonal signaling cascades interact to control the development and physiology of fleshy fruits. By applying a mutant-based approach, this study investigated the potential interconnection among light, auxin and ethylene signaling cascades during tomato fruit ripening and carotenogenesis. Analysis of ethylene and auxin metabolism and signaling in ripening fruits of the light-hyperresponsive high-pigment 2 (hp2) mutant revealed that the loss of HP2 function promotes the transcription of genes encoding key regulators of fruit ripening and increases ethylene signaling along with the increments in carotenoid synthesis and accumulation typically found in this mutant. Compared to the wild type (WT), significant changes in fruit auxin signaling were also observed in the hp2 mutant, including significantly higher activation of the auxin-responsive promoter DR5, severe down-regulation of all AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) genes more closely associated with fruit ripening as well as disturbed transcript abundance of genes encoding AUXIN RESPONSE FACTOR (ARF) transcription factors. Evidence of increased tissue responsivity to ethylene and auxins in hp2 ripening fruits is also provided. Moreover, comparing the auxin and ethylene metabolism and signaling in fruits of the phytochrome chromophore-deficient mutant aurea (au) in relation to the WT genotype provided new insights into the phytochrome-hormonal signaling crosstalk regulating the timing of fruit ripening. Compared to the WT, fruits of the au mutant exhibited a delayed-ripening phenotype, which was associated with the late induction of genes encoding master controllers of ripening, delayed ethylene climacteric production as well as coordinated changes in the expression of auxin signaling-related genes. Besides the temporal changes in hormonal signaling associated with ripening, the deficiency in functional phytochromes also seems to repress the cyclization of lycopene, leading to reduced levels of ?-carotene and lutein in the fruit tissues. Although the exact molecular mechanisms behind the altered hormonal responses in tomato fruits triggered by changes in light signaling remain to be further elucidated, the data obtained in this study provide clear evidence that an intricate crosstalk among light, ethylene and auxin signaling may be involved in controlling tomato fruit ripening and carotenogenesis. Therefore, these findings open up a window of opportunity for further improvement in the regulation of ripening-associated processes through the combined manipulation of hormonal and light signaling-related genes
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spelling Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesisInteração entre luz, etileno e auxinas durante o amadurecimento e carotenogênese em frutos de tomateiroAmadurecimento de frutosAuxinasAuxinsEthyleneEtilenoFruit ripeningLightLuzFruit ripening is a highly coordinated process involving numerous structural, biochemical and physiological changes, many of which are influenced by both endogenous and environmental stimuli. Light signaling and plant hormones such as ethylene and auxins have been identified as important regulators of tomato fruit ripening. However, it is still not fully understood how light and hormonal signaling cascades interact to control the development and physiology of fleshy fruits. By applying a mutant-based approach, this study investigated the potential interconnection among light, auxin and ethylene signaling cascades during tomato fruit ripening and carotenogenesis. Analysis of ethylene and auxin metabolism and signaling in ripening fruits of the light-hyperresponsive high-pigment 2 (hp2) mutant revealed that the loss of HP2 function promotes the transcription of genes encoding key regulators of fruit ripening and increases ethylene signaling along with the increments in carotenoid synthesis and accumulation typically found in this mutant. Compared to the wild type (WT), significant changes in fruit auxin signaling were also observed in the hp2 mutant, including significantly higher activation of the auxin-responsive promoter DR5, severe down-regulation of all AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) genes more closely associated with fruit ripening as well as disturbed transcript abundance of genes encoding AUXIN RESPONSE FACTOR (ARF) transcription factors. Evidence of increased tissue responsivity to ethylene and auxins in hp2 ripening fruits is also provided. Moreover, comparing the auxin and ethylene metabolism and signaling in fruits of the phytochrome chromophore-deficient mutant aurea (au) in relation to the WT genotype provided new insights into the phytochrome-hormonal signaling crosstalk regulating the timing of fruit ripening. Compared to the WT, fruits of the au mutant exhibited a delayed-ripening phenotype, which was associated with the late induction of genes encoding master controllers of ripening, delayed ethylene climacteric production as well as coordinated changes in the expression of auxin signaling-related genes. Besides the temporal changes in hormonal signaling associated with ripening, the deficiency in functional phytochromes also seems to repress the cyclization of lycopene, leading to reduced levels of ?-carotene and lutein in the fruit tissues. Although the exact molecular mechanisms behind the altered hormonal responses in tomato fruits triggered by changes in light signaling remain to be further elucidated, the data obtained in this study provide clear evidence that an intricate crosstalk among light, ethylene and auxin signaling may be involved in controlling tomato fruit ripening and carotenogenesis. Therefore, these findings open up a window of opportunity for further improvement in the regulation of ripening-associated processes through the combined manipulation of hormonal and light signaling-related genesO amadurecimento de frutos é um processo altamente regulado que envolve várias mudanças estruturais, bioquímicas e fisiológicas, muitas das quais são influenciadas tanto por fatores endógenos quanto ambientais. O sinal luminoso, bem como os hormônios vegetais etileno e auxina têm se revelado importantes reguladores do amadurecimento de frutos. Porém, ainda não está totalmente esclarecido como as cascatas de sinalização luminosa e hormonal interagem a fim de controlar o desenvolvimento e a fisiologia dos frutos carnosos. O presente estudo teve como objetivo analisar as interações entre as cascatas de sinalização da luz, do etileno e das auxinas durante o amadurecimento e carotenogênese em frutos de tomateiro por meio do uso de mutantes fotomorfogênicos dessa espécie. As análises do metabolismo e sinalização do etileno e das auxinas em frutos do mutante high-pigment 2 (hp2), o qual apresenta respostas exageradas à luz, revelaram que a perda da função do gene HP2 resultou no aumento dos níveis de transcritos de genes que codificam os reguladores-chaves do processo de amadurecimento bem como um incremento na sinalização do etileno, sendo que essas mudanças estiveram atreladas ao maior acúmulo de carotenoides tipicamente encontrados neste mutante. Comparado ao genótipo selvagem, frutos do mutante hp2 também apresentaram uma elevação considerável na sinalização das auxinas, incluindo incrementos na ativação do promotor DR5, regulação negativa da maioria dos genes AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) envolvidos no amadurecimento do tomate, bem como alterações na abundância de transcritos dos genes que codificam os fatores de transcrição AUXIN RESPONSE FACTOR (ARF). Indícios obtidos também sugerem uma maior responsividade dos frutos de hp2 aos hormônios etileno e auxinas. Além disso, as análises do metabolismo e a sinalização das auxinas e do etileno realizadas em frutos do mutante aurea (au), deficiente na síntese do cromóforo dos fitocromos, indicaram que a interação entre esses fotorreceptores e fitormônios influencia o início do amadurecimento dos frutos de tomateiro. Os frutos deste mutante, quando comparados ao selvagem, exibiram um atraso no amadurecimento, o qual se mostrou temporalmente relacionado à indução tardia dos genes que controlam esse processo, ao atraso na produção climatérica do etileno, bem como associado a alterações nos níveis de transcritos de genes-chaves relacionados com a sinalização das auxinas. Além das mudanças temporais na sinalização hormonal associadas ao amadurecimento, os dados obtidos também sugerem que a deficiência em fitocromos funcionais reprime a ciclização do licopeno, levando a níveis reduzidos de ?-caroteno e luteína nos tecidos dos frutos. Embora os mecanismos moleculares responsáveis pelas alterações nas respostas hormonais desencadeadas pela luz ainda precisem ser melhor elucidados em frutos de tomateiro, os dados obtidos neste estudo forneceram evidências de que uma complexa interação entre a sinalização luminosa, do etileno e das auxinas estaria envolvida no controle do amadurecimento e carotenogênese nessa espécie. Portanto, estas descobertas trazem consigo oportunidades de melhoria na regulação de eventos relacionados ao processo de amadurecimento por meio da manipulação combinada de genes relacionados à sinalização luminosa e hormonalBiblioteca Digitais de Teses e Dissertações da USPFreschi, LucianoCruz, Aline Bertinatto2017-06-26info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/doctoralThesisapplication/pdfhttp://www.teses.usp.br/teses/disponiveis/41/41132/tde-05092017-104106/reponame:Biblioteca Digital de Teses e Dissertações da USPinstname:Universidade de São Paulo (USP)instacron:USPLiberar o conteúdo para acesso público.info:eu-repo/semantics/openAccesseng2019-09-05T06:00:05Zoai:teses.usp.br:tde-05092017-104106Biblioteca Digital de Teses e Dissertaçõeshttp://www.teses.usp.br/PUBhttp://www.teses.usp.br/cgi-bin/mtd2br.plvirginia@if.usp.br|| atendimento@aguia.usp.br||virginia@if.usp.bropendoar:27212019-09-05T06:00:05Biblioteca Digital de Teses e Dissertações da USP - Universidade de São Paulo (USP)false
dc.title.none.fl_str_mv Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
Interação entre luz, etileno e auxinas durante o amadurecimento e carotenogênese em frutos de tomateiro
title Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
spellingShingle Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
Cruz, Aline Bertinatto
Amadurecimento de frutos
Auxinas
Auxins
Ethylene
Etileno
Fruit ripening
Light
Luz
title_short Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
title_full Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
title_fullStr Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
title_full_unstemmed Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
title_sort Light, ethylene and auxin crosstalk during tomato fruit ripening and carotenogenesis
author Cruz, Aline Bertinatto
author_facet Cruz, Aline Bertinatto
author_role author
dc.contributor.none.fl_str_mv Freschi, Luciano
dc.contributor.author.fl_str_mv Cruz, Aline Bertinatto
dc.subject.por.fl_str_mv Amadurecimento de frutos
Auxinas
Auxins
Ethylene
Etileno
Fruit ripening
Light
Luz
topic Amadurecimento de frutos
Auxinas
Auxins
Ethylene
Etileno
Fruit ripening
Light
Luz
description Fruit ripening is a highly coordinated process involving numerous structural, biochemical and physiological changes, many of which are influenced by both endogenous and environmental stimuli. Light signaling and plant hormones such as ethylene and auxins have been identified as important regulators of tomato fruit ripening. However, it is still not fully understood how light and hormonal signaling cascades interact to control the development and physiology of fleshy fruits. By applying a mutant-based approach, this study investigated the potential interconnection among light, auxin and ethylene signaling cascades during tomato fruit ripening and carotenogenesis. Analysis of ethylene and auxin metabolism and signaling in ripening fruits of the light-hyperresponsive high-pigment 2 (hp2) mutant revealed that the loss of HP2 function promotes the transcription of genes encoding key regulators of fruit ripening and increases ethylene signaling along with the increments in carotenoid synthesis and accumulation typically found in this mutant. Compared to the wild type (WT), significant changes in fruit auxin signaling were also observed in the hp2 mutant, including significantly higher activation of the auxin-responsive promoter DR5, severe down-regulation of all AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) genes more closely associated with fruit ripening as well as disturbed transcript abundance of genes encoding AUXIN RESPONSE FACTOR (ARF) transcription factors. Evidence of increased tissue responsivity to ethylene and auxins in hp2 ripening fruits is also provided. Moreover, comparing the auxin and ethylene metabolism and signaling in fruits of the phytochrome chromophore-deficient mutant aurea (au) in relation to the WT genotype provided new insights into the phytochrome-hormonal signaling crosstalk regulating the timing of fruit ripening. Compared to the WT, fruits of the au mutant exhibited a delayed-ripening phenotype, which was associated with the late induction of genes encoding master controllers of ripening, delayed ethylene climacteric production as well as coordinated changes in the expression of auxin signaling-related genes. Besides the temporal changes in hormonal signaling associated with ripening, the deficiency in functional phytochromes also seems to repress the cyclization of lycopene, leading to reduced levels of ?-carotene and lutein in the fruit tissues. Although the exact molecular mechanisms behind the altered hormonal responses in tomato fruits triggered by changes in light signaling remain to be further elucidated, the data obtained in this study provide clear evidence that an intricate crosstalk among light, ethylene and auxin signaling may be involved in controlling tomato fruit ripening and carotenogenesis. Therefore, these findings open up a window of opportunity for further improvement in the regulation of ripening-associated processes through the combined manipulation of hormonal and light signaling-related genes
publishDate 2017
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dc.rights.driver.fl_str_mv Liberar o conteúdo para acesso público.
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reponame:Biblioteca Digital de Teses e Dissertações da USP
instname:Universidade de São Paulo (USP)
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