Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms

Summary Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown...

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Veröffentlicht in:The Plant journal : for cell and molecular biology 2020-06, Vol.102 (5), p.1026-1041
Hauptverfasser: Barro‐Trastoy, Daniela, Carrera, Esther, Baños, Jorge, Palau‐Rodríguez, Julia, Ruiz‐Rivero, Omar, Tornero, Pablo, Alonso, José M., López‐Díaz, Isabel, Gómez, María Dolores, Pérez‐Amador, Miguel A.
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container_issue 5
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container_title The Plant journal : for cell and molecular biology
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creator Barro‐Trastoy, Daniela
Carrera, Esther
Baños, Jorge
Palau‐Rodríguez, Julia
Ruiz‐Rivero, Omar
Tornero, Pablo
Alonso, José M.
López‐Díaz, Isabel
Gómez, María Dolores
Pérez‐Amador, Miguel A.
description Summary Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity. Significance Statement The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation.
doi_str_mv 10.1111/tpj.14684
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In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity. Significance Statement The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14684</identifier><identifier>PMID: 31930587</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biosynthesis ; Brassinosteroids ; Brassinosteroids - metabolism ; Complexity ; Cytokinins ; Flowers &amp; plants ; Gene Expression Regulation, Plant - genetics ; Gene Expression Regulation, Plant - physiology ; Genetic analysis ; Gibberellins ; Gibberellins - metabolism ; hormone interaction ; Hormones ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - metabolism ; Molecular modelling ; ovule ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant species ; Primordia ; reproductive development ; Seeds ; Signal transduction ; Signal Transduction - genetics ; Signal Transduction - physiology ; Solanum lycopersicum ; tomato ; Tomatoes</subject><ispartof>The Plant journal : for cell and molecular biology, 2020-06, Vol.102 (5), p.1026-1041</ispartof><rights>2020 The Authors. 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In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity. Significance Statement The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. 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Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity. Significance Statement The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. 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subjects Arabidopsis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biosynthesis
Brassinosteroids
Brassinosteroids - metabolism
Complexity
Cytokinins
Flowers & plants
Gene Expression Regulation, Plant - genetics
Gene Expression Regulation, Plant - physiology
Genetic analysis
Gibberellins
Gibberellins - metabolism
hormone interaction
Hormones
Lycopersicon esculentum - genetics
Lycopersicon esculentum - metabolism
Molecular modelling
ovule
Plant Proteins - genetics
Plant Proteins - metabolism
Plant species
Primordia
reproductive development
Seeds
Signal transduction
Signal Transduction - genetics
Signal Transduction - physiology
Solanum lycopersicum
tomato
Tomatoes
title Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms
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