Ethylene-Related Gene Expression Networks in Wood Formation

Thickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Sig...

Full description

Bibliographic Details
Main Authors: Carolin Seyfferth, Bernard Wessels, Soile Jokipii-Lukkari, Björn Sundberg, Nicolas Delhomme, Judith Felten, Hannele Tuominen
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2018.00272/full
_version_ 1811213873414406144
author Carolin Seyfferth
Bernard Wessels
Soile Jokipii-Lukkari
Björn Sundberg
Nicolas Delhomme
Judith Felten
Hannele Tuominen
author_facet Carolin Seyfferth
Bernard Wessels
Soile Jokipii-Lukkari
Björn Sundberg
Nicolas Delhomme
Judith Felten
Hannele Tuominen
author_sort Carolin Seyfferth
collection DOAJ
description Thickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Signaling and transcriptional reprogramming by the phytohormone ethylene modifies cambial growth and cell differentiation, but the molecular link between ethylene and secondary growth remains unknown. We addressed this shortcoming by analyzing expression profiles and co-expression networks of ethylene pathway genes using the AspWood transcriptome database which covers all stages of secondary growth in aspen (Populus tremula) stems. ACC synthase expression suggests that the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized during xylem expansion and xylem cell maturation. Ethylene-mediated transcriptional reprogramming occurs during all stages of secondary growth, as deduced from AspWood expression profiles of ethylene-responsive genes. A network centrality analysis of the AspWood dataset identified EIN3D and 11 ERFs as hubs. No overlap was found between the co-expressed genes of the EIN3 and ERF hubs, suggesting target diversification and hence independent roles for these transcription factor families during normal wood formation. The EIN3D hub was part of a large co-expression gene module, which contained 16 transcription factors, among them several new candidates that have not been earlier connected to wood formation and a VND-INTERACTING 2 (VNI2) homolog. We experimentally demonstrated Populus EIN3D function in ethylene signaling in Arabidopsis thaliana. The ERF hubs ERF118 and ERF119 were connected on the basis of their expression pattern and gene co-expression module composition to xylem cell expansion and secondary cell wall formation, respectively. We hereby establish data resources for ethylene-responsive genes and potential targets for EIN3D and ERF transcription factors in Populus stem tissues, which can help to understand the range of ethylene targeted biological processes during secondary growth.
first_indexed 2024-04-12T05:53:37Z
format Article
id doaj.art-1413be6dff284c59aa62ffaac5a2741e
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-04-12T05:53:37Z
publishDate 2018-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-1413be6dff284c59aa62ffaac5a2741e2022-12-22T03:45:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-03-01910.3389/fpls.2018.00272322906Ethylene-Related Gene Expression Networks in Wood FormationCarolin Seyfferth0Bernard Wessels1Soile Jokipii-Lukkari2Björn Sundberg3Nicolas Delhomme4Judith Felten5Hannele Tuominen6Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, SwedenDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, SwedenDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, SwedenDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, SwedenDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, SwedenDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, SwedenDepartment of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, SwedenThickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Signaling and transcriptional reprogramming by the phytohormone ethylene modifies cambial growth and cell differentiation, but the molecular link between ethylene and secondary growth remains unknown. We addressed this shortcoming by analyzing expression profiles and co-expression networks of ethylene pathway genes using the AspWood transcriptome database which covers all stages of secondary growth in aspen (Populus tremula) stems. ACC synthase expression suggests that the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized during xylem expansion and xylem cell maturation. Ethylene-mediated transcriptional reprogramming occurs during all stages of secondary growth, as deduced from AspWood expression profiles of ethylene-responsive genes. A network centrality analysis of the AspWood dataset identified EIN3D and 11 ERFs as hubs. No overlap was found between the co-expressed genes of the EIN3 and ERF hubs, suggesting target diversification and hence independent roles for these transcription factor families during normal wood formation. The EIN3D hub was part of a large co-expression gene module, which contained 16 transcription factors, among them several new candidates that have not been earlier connected to wood formation and a VND-INTERACTING 2 (VNI2) homolog. We experimentally demonstrated Populus EIN3D function in ethylene signaling in Arabidopsis thaliana. The ERF hubs ERF118 and ERF119 were connected on the basis of their expression pattern and gene co-expression module composition to xylem cell expansion and secondary cell wall formation, respectively. We hereby establish data resources for ethylene-responsive genes and potential targets for EIN3D and ERF transcription factors in Populus stem tissues, which can help to understand the range of ethylene targeted biological processes during secondary growth.http://journal.frontiersin.org/article/10.3389/fpls.2018.00272/fullethylene signalingsecondary growthwood developmentco-expression networkEIN3ERF
spellingShingle Carolin Seyfferth
Bernard Wessels
Soile Jokipii-Lukkari
Björn Sundberg
Nicolas Delhomme
Judith Felten
Hannele Tuominen
Ethylene-Related Gene Expression Networks in Wood Formation
Frontiers in Plant Science
ethylene signaling
secondary growth
wood development
co-expression network
EIN3
ERF
title Ethylene-Related Gene Expression Networks in Wood Formation
title_full Ethylene-Related Gene Expression Networks in Wood Formation
title_fullStr Ethylene-Related Gene Expression Networks in Wood Formation
title_full_unstemmed Ethylene-Related Gene Expression Networks in Wood Formation
title_short Ethylene-Related Gene Expression Networks in Wood Formation
title_sort ethylene related gene expression networks in wood formation
topic ethylene signaling
secondary growth
wood development
co-expression network
EIN3
ERF
url http://journal.frontiersin.org/article/10.3389/fpls.2018.00272/full
work_keys_str_mv AT carolinseyfferth ethylenerelatedgeneexpressionnetworksinwoodformation
AT bernardwessels ethylenerelatedgeneexpressionnetworksinwoodformation
AT soilejokipiilukkari ethylenerelatedgeneexpressionnetworksinwoodformation
AT bjornsundberg ethylenerelatedgeneexpressionnetworksinwoodformation
AT nicolasdelhomme ethylenerelatedgeneexpressionnetworksinwoodformation
AT judithfelten ethylenerelatedgeneexpressionnetworksinwoodformation
AT hanneletuominen ethylenerelatedgeneexpressionnetworksinwoodformation