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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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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