A Robust Auxin Response Network Controls Embryo and Suspensor Development through a bHLH Transcriptional Module

Tatyana Radoeva, Annemarie S. Lokerse, Cristina I. Llavata-Peris, Jos Wendrich, Daoquan Xiang, Che-Yang Liao, Lieke Vlaar, Mark Boekschoten, Guido Hooiveld, Raju Datla, Dolf Weijers

Research output: Contribution to journalArticleAcademicpeer-review

5 Citations (Scopus)

Abstract

Land plants can reproduce sexually by developing an embryo from a fertilized egg cell. However, embryos can also be formed from other cell types in many plant species. A key question is thus how embryo identity in plants is controlled, and how this process is modified during non-zygotic embryogenesis. The Arabidopsis zygote divides to produce an embryonic lineage and an extra-embryonic suspensor. Yet, normally quiescent suspensor cells can develop a second embryo when the initial embryo is damaged, or when response to the signaling molecule auxin is locally blocked. Here we have used auxin-dependent suspensor embryogenesis as a model to determine transcriptome changes during embryonic reprogramming. We find that reprogramming is complex and accompanied by large transcriptomic changes prior to anatomic changes. This analysis revealed a strong enrichment for genes encoding components of auxin homeostasis and response among misregulated genes. Strikingly, deregulation among multiple auxin-related gene families converged upon re-establishment of cellular auxin levels or response. This suggests a remarkable degree of feedback regulation to create resilience in auxin response during embryo development. Starting from the transcriptome of auxin-deregulated embryos, we identify an auxin-dependent bHLH transcription factor network that mediates the activity of this hormone in suppressing embryo development from the suspensor.
LanguageEnglish
Pages52-67
JournalThe Plant Cell
Volume31
Early online date20 Dec 2018
DOIs
Publication statusPublished - Jan 2019

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Indoleacetic Acids
embryo (plant)
Embryonic Development
auxins
Embryonic Structures
embryogenesis
Zygote
Transcriptome
transcriptome
Embryophyta
Gene Components
Basic Helix-Loop-Helix Transcription Factors
genes
embryophytes
zygote
ova
transcriptomics
Arabidopsis
Genes
homeostasis

Cite this

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title = "A Robust Auxin Response Network Controls Embryo and Suspensor Development through a bHLH Transcriptional Module",
abstract = "Land plants can reproduce sexually by developing an embryo from a fertilized egg cell. However, embryos can also be formed from other cell types in many plant species. A key question is thus how embryo identity in plants is controlled, and how this process is modified during non-zygotic embryogenesis. The Arabidopsis zygote divides to produce an embryonic lineage and an extra-embryonic suspensor. Yet, normally quiescent suspensor cells can develop a second embryo when the initial embryo is damaged, or when response to the signaling molecule auxin is locally blocked. Here we have used auxin-dependent suspensor embryogenesis as a model to determine transcriptome changes during embryonic reprogramming. We find that reprogramming is complex and accompanied by large transcriptomic changes prior to anatomic changes. This analysis revealed a strong enrichment for genes encoding components of auxin homeostasis and response among misregulated genes. Strikingly, deregulation among multiple auxin-related gene families converged upon re-establishment of cellular auxin levels or response. This suggests a remarkable degree of feedback regulation to create resilience in auxin response during embryo development. Starting from the transcriptome of auxin-deregulated embryos, we identify an auxin-dependent bHLH transcription factor network that mediates the activity of this hormone in suppressing embryo development from the suspensor.",
author = "Tatyana Radoeva and Lokerse, {Annemarie S.} and Llavata-Peris, {Cristina I.} and Jos Wendrich and Daoquan Xiang and Che-Yang Liao and Lieke Vlaar and Mark Boekschoten and Guido Hooiveld and Raju Datla and Dolf Weijers",
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A Robust Auxin Response Network Controls Embryo and Suspensor Development through a bHLH Transcriptional Module. / Radoeva, Tatyana; Lokerse, Annemarie S.; Llavata-Peris, Cristina I.; Wendrich, Jos; Xiang, Daoquan; Liao, Che-Yang; Vlaar, Lieke; Boekschoten, Mark; Hooiveld, Guido; Datla, Raju; Weijers, Dolf.

In: The Plant Cell, Vol. 31, 01.2019, p. 52-67.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Radoeva, Tatyana

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AU - Wendrich, Jos

AU - Xiang, Daoquan

AU - Liao, Che-Yang

AU - Vlaar, Lieke

AU - Boekschoten, Mark

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AU - Datla, Raju

AU - Weijers, Dolf

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AB - Land plants can reproduce sexually by developing an embryo from a fertilized egg cell. However, embryos can also be formed from other cell types in many plant species. A key question is thus how embryo identity in plants is controlled, and how this process is modified during non-zygotic embryogenesis. The Arabidopsis zygote divides to produce an embryonic lineage and an extra-embryonic suspensor. Yet, normally quiescent suspensor cells can develop a second embryo when the initial embryo is damaged, or when response to the signaling molecule auxin is locally blocked. Here we have used auxin-dependent suspensor embryogenesis as a model to determine transcriptome changes during embryonic reprogramming. We find that reprogramming is complex and accompanied by large transcriptomic changes prior to anatomic changes. This analysis revealed a strong enrichment for genes encoding components of auxin homeostasis and response among misregulated genes. Strikingly, deregulation among multiple auxin-related gene families converged upon re-establishment of cellular auxin levels or response. This suggests a remarkable degree of feedback regulation to create resilience in auxin response during embryo development. Starting from the transcriptome of auxin-deregulated embryos, we identify an auxin-dependent bHLH transcription factor network that mediates the activity of this hormone in suppressing embryo development from the suspensor.

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