Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits

Detalhes bibliográficos
Autor(a) principal: Bianchetti, Ricardo Ernesto
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-03042018-085522/
Resumo: Phytochromes (PHYs) and plant hormones have been emerging as important regulators of fleshy fruit physiology and quality traits; however, the relevance of PHY-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. This Thesis assesses the role of PHYs and their interplay with auxins, cytokinins and ethylene during the regulation of tomato (Solanum lycopersicum) fruit development and ripening, with a focus on the control of the plastid biogenesis, sugar metabolism and carotenoid accumulation. In Chapter I, we present evidence that the deficiency in PHY chromophore phytochromobilin (PΦB) biosynthesis, which leads to a global deficiency in functional PHYs, represses fruit chloroplast biogenesis in immature fruits and inhibits fruit sugar accumulation by transcriptionally downregulating sink- and starch biosynthesis-related enzymes. Genetic and physiological evidence suggested the involvement of both auxins and cytokinins as mediators of the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. During the ripening phase, PΦB deficiency was shown to delay the rise in climacteric ethylene production, affecting the ripening initiation rather than its progression. PHY-hormonal signaling crosstalk was shown to be active not only in the more externally positioned fruit tissues (i.e., pericarp) but also in the most inner fruit regions (i.e., columella). We, therefore, concluded that the global deficiency in functional PHY drastically affects fruit sugar metabolism, chloroplast formation as well as the timing of ripening via an intricate interplay involving phytochromes, auxins, cytokinins and ethylene. In Chapter II, we employed fruit-specific RNAi-mediated silencing of PHY genes to shed light on the specific role played by fruit-localized PHYs and their downstream signaling cascades on tomato fruit physiology and quality traits. Data revealed that fruit-localized SlPHYB2 negatively regulates chlorophyll accumulation in immature fruits whereas SlPHYA positively influences the plastid division machinery. Both SlPHYA and SlPHYB2 were shown to play overlapping, yet distinct, roles in controlling fruit starch metabolism and carotenoid biosynthesis. Our data implicated cytokinin signaling-related proteins as mediators of the SlPHYA-dependent regulation of plastid division machinery, and specific AUXIN RESPONSE FACTORs as intermediates in the PHY-mediated regulation of fruit sugar and carotenoid metabolisms. We concluded that fruit-localized SlPHYA- and SlPHYB2-mediated light perception regulate fruit plastid biogenesis as well as sugar and carotenoid metabolisms via coordinated changes in key components of both auxin and cytokinin signaling cascades. Altogether, this study brings important insights into the combined action of PHYs and hormones in the control of fruit plastid biogenesis and highlights that the interplay between PHY-hormonal signaling cascades influences essential features of tomato fruit quality, such as the sugar and carotenoid accumulation
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spelling Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traitsInterações entre fitocromos e fitormônios em tomateiro: impactos na fisiologia e qualidade nutricional dos frutosAmidoAuxinAuxinaChloroplastCitocininaCloroplastoCytokininLight signalingSinalização luminosaStarchPhytochromes (PHYs) and plant hormones have been emerging as important regulators of fleshy fruit physiology and quality traits; however, the relevance of PHY-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. This Thesis assesses the role of PHYs and their interplay with auxins, cytokinins and ethylene during the regulation of tomato (Solanum lycopersicum) fruit development and ripening, with a focus on the control of the plastid biogenesis, sugar metabolism and carotenoid accumulation. In Chapter I, we present evidence that the deficiency in PHY chromophore phytochromobilin (PΦB) biosynthesis, which leads to a global deficiency in functional PHYs, represses fruit chloroplast biogenesis in immature fruits and inhibits fruit sugar accumulation by transcriptionally downregulating sink- and starch biosynthesis-related enzymes. Genetic and physiological evidence suggested the involvement of both auxins and cytokinins as mediators of the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. During the ripening phase, PΦB deficiency was shown to delay the rise in climacteric ethylene production, affecting the ripening initiation rather than its progression. PHY-hormonal signaling crosstalk was shown to be active not only in the more externally positioned fruit tissues (i.e., pericarp) but also in the most inner fruit regions (i.e., columella). We, therefore, concluded that the global deficiency in functional PHY drastically affects fruit sugar metabolism, chloroplast formation as well as the timing of ripening via an intricate interplay involving phytochromes, auxins, cytokinins and ethylene. In Chapter II, we employed fruit-specific RNAi-mediated silencing of PHY genes to shed light on the specific role played by fruit-localized PHYs and their downstream signaling cascades on tomato fruit physiology and quality traits. Data revealed that fruit-localized SlPHYB2 negatively regulates chlorophyll accumulation in immature fruits whereas SlPHYA positively influences the plastid division machinery. Both SlPHYA and SlPHYB2 were shown to play overlapping, yet distinct, roles in controlling fruit starch metabolism and carotenoid biosynthesis. Our data implicated cytokinin signaling-related proteins as mediators of the SlPHYA-dependent regulation of plastid division machinery, and specific AUXIN RESPONSE FACTORs as intermediates in the PHY-mediated regulation of fruit sugar and carotenoid metabolisms. We concluded that fruit-localized SlPHYA- and SlPHYB2-mediated light perception regulate fruit plastid biogenesis as well as sugar and carotenoid metabolisms via coordinated changes in key components of both auxin and cytokinin signaling cascades. Altogether, this study brings important insights into the combined action of PHYs and hormones in the control of fruit plastid biogenesis and highlights that the interplay between PHY-hormonal signaling cascades influences essential features of tomato fruit quality, such as the sugar and carotenoid accumulationFitocromos (PHYs) e fitormônios têm sido caracterizados como importantes reguladores da fisiologia e qualidade de frutos carnosos; todavia, a importância de interações entre a sinalização hormonal e dos PHYs no controle do desenvolvimento e metabolismo de frutos ainda permanece pouco elucidada. Este trabalho de Tese avaliou o papel dos PHYs e das suas interações com as auxinas, as citocininas e o etileno sobre a regulação do desenvolvimento e amadurecimento de frutos de tomateiro (Solanum lycopersicum), particularmente no que tange ao controle da biogênese plastidial e metabolismos de açúcares e de carotenoides. No Capítulo I são apresentadas evidências de que a deficiência na produção de fitocromobilina (PΦB), a qual resulta numa deficiência global in PHYs funcionais, impacta negativamente a biogênese de cloroplastos em frutos imaturos e inibe o acúmulo de açúcares por meio da repressão transcricional de enzimas relacionadas a biossíntese de amido e força de dreno nos frutos. Evidências genéticas e fisiológicas indicaram o envolvimento tanto das auxinas quanto das citocininas como mediadoras do impacto negativo da deficiência de PΦB sobre a força de dreno dos frutos bem como na formação de cloroplastos. Durante a fase de amadurecimento, a deficiência em PΦB atrasou a produção climatérica de etileno, afetando o início do amadurecimento mas não a sua progressão. As interações entre PHYs e hormônios mostraram-se ativas não apenas nos tecidos posicionados mais externamente (i.e., pericarpo) mas também nas regiões mais internas do fruto (i.e., columela). Conclui-se, portanto, que a deficiência global em PHYs funcionais afeta drasticamente o metabolismo de açucares, formação de cloroplastos, bem como o tempo de amadurecimento através de uma interação complexa envolvendo fitocromos, auxinas, citocininas e etileno. No Capítulo II utilizamos o silenciamento fruto-específico de PHYs a fim de desvendar de que forma a fisiologia e parâmetros de qualidade do tomate seriam regulados por PHYs presentes no próprio fruto. Os dados obtidos revelaram que moléculas de SlPHYB2 presentes no próprio fruto regulam negativamente o acúmulo de clorofilas nos frutos imaturos, já as de SlPHYA influenciam positivamente a maquinaria de divisão plastidial, e tanto SlPHYA quanto SlPHYB2 desempenham papel sobrepostos, porém distintos, no controle do metabolismo de amido e acúmulo de carotenoides em frutos de tomateiro. Evidências sugerem que proteínas relacionadas à sinalização de citocininas atuariam como mediadoras do impacto de SlPHYA sobre a maquinaria de divisão plastidial, e que AUXIN RESPONSE FACTORs específicos seriam intermediários no controle dos PHYs sobre os metabolismos de açúcares e carotenoides. Conclui-se, dessa forma, que a percepção de luz mediada por moléculas de SlPHYA e SlPHYB2 presentes no próprio fruto regulam a biogênese plastidial e os metabolismos de açúcares e carotenoides por meio de alterações coordenadas em componentes chaves das cascatas de sinalização de auxinas e citocininas. Quando combinados, os dados obtidos neste estudo apresentam novidades importantes sobre a ação conjunta de PHYs e fitormônios no controle da biogênese plastidial e demonstram que a interação entre esses sinalizadores influencia características essenciais da qualidade de frutos de tomateiro, tais como o acúmulo de açúcares e de carotenoidesBiblioteca Digitais de Teses e Dissertações da USPFreschi, LucianoRossi, Maria MagdalenaBianchetti, Ricardo Ernesto2017-12-12info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/doctoralThesisapplication/pdfhttp://www.teses.usp.br/teses/disponiveis/41/41132/tde-03042018-085522/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/openAccesseng2018-07-19T20:50:39Zoai:teses.usp.br:tde-03042018-085522Biblioteca 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:27212018-07-19T20:50:39Biblioteca Digital de Teses e Dissertações da USP - Universidade de São Paulo (USP)false
dc.title.none.fl_str_mv Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
Interações entre fitocromos e fitormônios em tomateiro: impactos na fisiologia e qualidade nutricional dos frutos
title Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
spellingShingle Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
Bianchetti, Ricardo Ernesto
Amido
Auxin
Auxina
Chloroplast
Citocinina
Cloroplasto
Cytokinin
Light signaling
Sinalização luminosa
Starch
title_short Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
title_full Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
title_fullStr Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
title_full_unstemmed Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
title_sort Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits
author Bianchetti, Ricardo Ernesto
author_facet Bianchetti, Ricardo Ernesto
author_role author
dc.contributor.none.fl_str_mv Freschi, Luciano
Rossi, Maria Magdalena
dc.contributor.author.fl_str_mv Bianchetti, Ricardo Ernesto
dc.subject.por.fl_str_mv Amido
Auxin
Auxina
Chloroplast
Citocinina
Cloroplasto
Cytokinin
Light signaling
Sinalização luminosa
Starch
topic Amido
Auxin
Auxina
Chloroplast
Citocinina
Cloroplasto
Cytokinin
Light signaling
Sinalização luminosa
Starch
description Phytochromes (PHYs) and plant hormones have been emerging as important regulators of fleshy fruit physiology and quality traits; however, the relevance of PHY-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. This Thesis assesses the role of PHYs and their interplay with auxins, cytokinins and ethylene during the regulation of tomato (Solanum lycopersicum) fruit development and ripening, with a focus on the control of the plastid biogenesis, sugar metabolism and carotenoid accumulation. In Chapter I, we present evidence that the deficiency in PHY chromophore phytochromobilin (PΦB) biosynthesis, which leads to a global deficiency in functional PHYs, represses fruit chloroplast biogenesis in immature fruits and inhibits fruit sugar accumulation by transcriptionally downregulating sink- and starch biosynthesis-related enzymes. Genetic and physiological evidence suggested the involvement of both auxins and cytokinins as mediators of the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. During the ripening phase, PΦB deficiency was shown to delay the rise in climacteric ethylene production, affecting the ripening initiation rather than its progression. PHY-hormonal signaling crosstalk was shown to be active not only in the more externally positioned fruit tissues (i.e., pericarp) but also in the most inner fruit regions (i.e., columella). We, therefore, concluded that the global deficiency in functional PHY drastically affects fruit sugar metabolism, chloroplast formation as well as the timing of ripening via an intricate interplay involving phytochromes, auxins, cytokinins and ethylene. In Chapter II, we employed fruit-specific RNAi-mediated silencing of PHY genes to shed light on the specific role played by fruit-localized PHYs and their downstream signaling cascades on tomato fruit physiology and quality traits. Data revealed that fruit-localized SlPHYB2 negatively regulates chlorophyll accumulation in immature fruits whereas SlPHYA positively influences the plastid division machinery. Both SlPHYA and SlPHYB2 were shown to play overlapping, yet distinct, roles in controlling fruit starch metabolism and carotenoid biosynthesis. Our data implicated cytokinin signaling-related proteins as mediators of the SlPHYA-dependent regulation of plastid division machinery, and specific AUXIN RESPONSE FACTORs as intermediates in the PHY-mediated regulation of fruit sugar and carotenoid metabolisms. We concluded that fruit-localized SlPHYA- and SlPHYB2-mediated light perception regulate fruit plastid biogenesis as well as sugar and carotenoid metabolisms via coordinated changes in key components of both auxin and cytokinin signaling cascades. Altogether, this study brings important insights into the combined action of PHYs and hormones in the control of fruit plastid biogenesis and highlights that the interplay between PHY-hormonal signaling cascades influences essential features of tomato fruit quality, such as the sugar and carotenoid accumulation
publishDate 2017
dc.date.none.fl_str_mv 2017-12-12
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/doctoralThesis
format doctoralThesis
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://www.teses.usp.br/teses/disponiveis/41/41132/tde-03042018-085522/
url http://www.teses.usp.br/teses/disponiveis/41/41132/tde-03042018-085522/
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv
dc.rights.driver.fl_str_mv Liberar o conteúdo para acesso público.
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Liberar o conteúdo para acesso público.
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
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dc.publisher.none.fl_str_mv Biblioteca Digitais de Teses e Dissertações da USP
publisher.none.fl_str_mv Biblioteca Digitais de Teses e Dissertações da USP
dc.source.none.fl_str_mv
reponame:Biblioteca Digital de Teses e Dissertações da USP
instname:Universidade de São Paulo (USP)
instacron:USP
instname_str Universidade de São Paulo (USP)
instacron_str USP
institution USP
reponame_str Biblioteca Digital de Teses e Dissertações da USP
collection Biblioteca Digital de Teses e Dissertações da USP
repository.name.fl_str_mv Biblioteca Digital de Teses e Dissertações da USP - Universidade de São Paulo (USP)
repository.mail.fl_str_mv virginia@if.usp.br|| atendimento@aguia.usp.br||virginia@if.usp.br
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