Redundancy, feedback, and robustness in the Arabidopsis thaliana BZR/BEH gene family

Abstract

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 BRZ/BEH gene family, whose function is crucial for embryonic stem development in the plant Arabidopsis thaliana, to test current assumptions on functional redundancy and trait robustness. Our analyses of BRZ/BEH gene mutants and mutant combinations revealed that functional redundancy among gene family members does not contribute to 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 robustness. Instead, we found that only BEH4, the most ancient family member, modulated developmental robustness. We present evidence that regulatory cross-talk among gene family members is integrated by BEH4 and promotes 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.