Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family

Organismal development is remarkably robust, tolerating stochastic errors to produce consistent, so-called canalized adult phenotypes. The mechanistic underpinnings of developmental robustness are poorly understood, but recent studies implicate certain features of genetic networks such as functional...

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Main Authors: Jennifer Lachowiec, G. Alex Mason, Karla Schultz, Christine Queitsch
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2018.00523/full
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spelling doaj-de4d059d26084c4a80c864dba21b6a2d2020-11-24T21:40:44ZengFrontiers Media S.A.Frontiers in Genetics1664-80212018-11-01910.3389/fgene.2018.00523419247Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene FamilyJennifer Lachowiec0Jennifer Lachowiec1G. Alex Mason2Karla Schultz3Christine Queitsch4Department of Genome Sciences, University of Washington, Seattle, WA, United StatesMolecular and Cellular Biology Program, University of Washington, Seattle, WA, United StatesDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesDepartment of Genome Sciences, University of Washington, Seattle, WA, United StatesOrganismal development is remarkably robust, tolerating stochastic errors to produce consistent, so-called canalized adult phenotypes. The mechanistic underpinnings of developmental robustness are poorly understood, but recent studies implicate certain features of genetic networks such as functional redundancy, connectivity, and feedback. Here, we examine the BZR/BEH gene family, whose function contributes to embryonic stem development in the plant Arabidopsis thaliana, to test current assumptions on functional redundancy and trait robustness. Our analyses of BZR/BEH gene mutants and mutant combinations revealed that functional redundancy among these gene family members is not necessary for trait robustness. Connectivity is another commonly cited determinant of robustness; however, we found no correlation between connectivity among gene family members or their connectivity with other transcription factors and effects on developmental robustness. Instead, our data suggest that BEH4, the earliest diverged family member, modulates developmental robustness. We present evidence indicating that regulatory cross-talk among gene family members is integrated by BEH4 to promote wild-type levels of developmental robustness. Further, the chaperone HSP90, a known determinant of developmental robustness, appears to act via BEH4 in maintaining robustness of embryonic stem length. In summary, we demonstrate that even among closely related transcription factors, trait robustness can arise through the activity of a single gene family member, challenging common assumptions about the molecular underpinnings of robustness.https://www.frontiersin.org/article/10.3389/fgene.2018.00523/fulldevelopmental robustnessstochasticitycanalizationplanthypocotylvariance
collection DOAJ
language English
format Article
sources DOAJ
author Jennifer Lachowiec
Jennifer Lachowiec
G. Alex Mason
Karla Schultz
Christine Queitsch
spellingShingle Jennifer Lachowiec
Jennifer Lachowiec
G. Alex Mason
Karla Schultz
Christine Queitsch
Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
Frontiers in Genetics
developmental robustness
stochasticity
canalization
plant
hypocotyl
variance
author_facet Jennifer Lachowiec
Jennifer Lachowiec
G. Alex Mason
Karla Schultz
Christine Queitsch
author_sort Jennifer Lachowiec
title Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
title_short Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
title_full Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
title_fullStr Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
title_full_unstemmed Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
title_sort redundancy, feedback, and robustness in the arabidopsis thaliana bzr/beh gene family
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2018-11-01
description Organismal development is remarkably robust, tolerating stochastic errors to produce consistent, so-called canalized adult phenotypes. The mechanistic underpinnings of developmental robustness are poorly understood, but recent studies implicate certain features of genetic networks such as functional redundancy, connectivity, and feedback. Here, we examine the BZR/BEH gene family, whose function contributes to embryonic stem development in the plant Arabidopsis thaliana, to test current assumptions on functional redundancy and trait robustness. Our analyses of BZR/BEH gene mutants and mutant combinations revealed that functional redundancy among these gene family members is not necessary for trait robustness. Connectivity is another commonly cited determinant of robustness; however, we found no correlation between connectivity among gene family members or their connectivity with other transcription factors and effects on developmental robustness. Instead, our data suggest that BEH4, the earliest diverged family member, modulates developmental robustness. We present evidence indicating that regulatory cross-talk among gene family members is integrated by BEH4 to promote wild-type levels of developmental robustness. Further, the chaperone HSP90, a known determinant of developmental robustness, appears to act via BEH4 in maintaining robustness of embryonic stem length. In summary, we demonstrate that even among closely related transcription factors, trait robustness can arise through the activity of a single gene family member, challenging common assumptions about the molecular underpinnings of robustness.
topic developmental robustness
stochasticity
canalization
plant
hypocotyl
variance
url https://www.frontiersin.org/article/10.3389/fgene.2018.00523/full
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