Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato

Most flowering plants must defend themselves against herbivores for survival and attract pollinators for reproduction. Although traits involved in plant defence and pollinator attraction are often localised in leaves and flowers, respectively, they will show a diffuse evolution if they share the sam...

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Main Authors: Lanlan Ke, Yangzi Wang, Martin Schäfer, Thomas Städler, Rensen Zeng, Jörg Fabian, Hannier Pulido, Consuelo M. De Moraes, Yuanyuan Song, Shuqing Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.722810/full
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spelling doaj-49d39d510104490dbcc82d59ba30f1c02021-09-22T14:06:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.722810722810Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in TomatoLanlan Ke0Lanlan Ke1Yangzi Wang2Martin Schäfer3Thomas Städler4Rensen Zeng5Jörg Fabian6Hannier Pulido7Consuelo M. De Moraes8Yuanyuan Song9Shuqing Xu10Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaInstitute for Evolution and Biodiversity, University of Münster, Münster, GermanyInstitute for Evolution and Biodiversity, University of Münster, Münster, GermanyInstitute for Evolution and Biodiversity, University of Münster, Münster, GermanyPlant Ecological Genetics Group, Institute of Integrative Biology, ETH Zürich, Zürich, SwitzerlandKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaInstitute for Pharmaceutical and Medicinal Chemistry, University of Münster, Münster, GermanyDepartment of Environmental Systems Sciences, ETH Zürich, Zürich, SwitzerlandDepartment of Environmental Systems Sciences, ETH Zürich, Zürich, SwitzerlandKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaInstitute for Evolution and Biodiversity, University of Münster, Münster, GermanyMost flowering plants must defend themselves against herbivores for survival and attract pollinators for reproduction. Although traits involved in plant defence and pollinator attraction are often localised in leaves and flowers, respectively, they will show a diffuse evolution if they share the same molecular machinery and regulatory networks. We performed RNA-sequencing to characterise and compare transcriptomic changes involved in herbivory-induced defences and flower development, in tomato leaves and flowers, respectively. We found that both the herbivory-induced responses and flower development involved alterations in jasmonic acid signalling, suppression of primary metabolism and reprogramming of secondary metabolism. We identified 411 genes that were involved in both processes, a number significantly higher than expected by chance. Genetic manipulation of key regulators of induced defences also led to the expression changes in the same genes in both leaves and flowers. Targeted metabolomic analysis showed that among closely related tomato species, jasmonic acid and α-tomatine are correlated in flower buds and herbivory-induced leaves. These findings suggest that herbivory-induced responses and flower development share a common molecular machinery and likely have coevolved in nature.https://www.frontiersin.org/articles/10.3389/fpls.2021.722810/fullherbivorydefence responseflower developmentpollinator attractionpleiotropyjasmonic acid
collection DOAJ
language English
format Article
sources DOAJ
author Lanlan Ke
Lanlan Ke
Yangzi Wang
Martin Schäfer
Thomas Städler
Rensen Zeng
Jörg Fabian
Hannier Pulido
Consuelo M. De Moraes
Yuanyuan Song
Shuqing Xu
spellingShingle Lanlan Ke
Lanlan Ke
Yangzi Wang
Martin Schäfer
Thomas Städler
Rensen Zeng
Jörg Fabian
Hannier Pulido
Consuelo M. De Moraes
Yuanyuan Song
Shuqing Xu
Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
Frontiers in Plant Science
herbivory
defence response
flower development
pollinator attraction
pleiotropy
jasmonic acid
author_facet Lanlan Ke
Lanlan Ke
Yangzi Wang
Martin Schäfer
Thomas Städler
Rensen Zeng
Jörg Fabian
Hannier Pulido
Consuelo M. De Moraes
Yuanyuan Song
Shuqing Xu
author_sort Lanlan Ke
title Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
title_short Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
title_full Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
title_fullStr Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
title_full_unstemmed Transcriptomic Profiling Reveals Shared Signalling Networks Between Flower Development and Herbivory-Induced Responses in Tomato
title_sort transcriptomic profiling reveals shared signalling networks between flower development and herbivory-induced responses in tomato
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-09-01
description Most flowering plants must defend themselves against herbivores for survival and attract pollinators for reproduction. Although traits involved in plant defence and pollinator attraction are often localised in leaves and flowers, respectively, they will show a diffuse evolution if they share the same molecular machinery and regulatory networks. We performed RNA-sequencing to characterise and compare transcriptomic changes involved in herbivory-induced defences and flower development, in tomato leaves and flowers, respectively. We found that both the herbivory-induced responses and flower development involved alterations in jasmonic acid signalling, suppression of primary metabolism and reprogramming of secondary metabolism. We identified 411 genes that were involved in both processes, a number significantly higher than expected by chance. Genetic manipulation of key regulators of induced defences also led to the expression changes in the same genes in both leaves and flowers. Targeted metabolomic analysis showed that among closely related tomato species, jasmonic acid and α-tomatine are correlated in flower buds and herbivory-induced leaves. These findings suggest that herbivory-induced responses and flower development share a common molecular machinery and likely have coevolved in nature.
topic herbivory
defence response
flower development
pollinator attraction
pleiotropy
jasmonic acid
url https://www.frontiersin.org/articles/10.3389/fpls.2021.722810/full
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