Structural variation affecting DNA backbone interactions underlies adaptation of B3 DNA binding domains to constraints imposed by protein architecture

Abstract

Functional and architectural diversification of transcription factor families has played a central role in the independent evolution of complex development in plants and animals. Here, we investigate the role of architectural constraints on evolution of B3 DNA binding domains that regulate plant embryogenesis. B3 domains of ABI3, FUS3, LEC2 and VAL1 proteins recognize the same cis-element. Complex architectures of ABI3 and VAL1 integrate cis-element recognition with other signals, whereas LEC2 and FUS3 have reduced architectures conducive to roles as pioneer activators. In yeast and plant in vivo assays, B3 domain functions correlate with architectural complexity of the parent transcription factor rather than phylogenetic relatedness. In a complex architecture, attenuated ABI3-B3 and VAL1-B3 activities enable integration of cis-element recognition with hormone signaling, whereas hyper-active LEC2-B3 and FUS3-B3 over-ride hormonal control. Three clade-specific amino acid substitutions (β4-triad) implicated in interactions with the DNA backbone account for divergence of LEC2-B3 and ABI3-B3. We find a striking correlation between differences in in vitro DNA binding affinity and in vivo activities of B3 domains in plants and yeast. Our results highlight the role of DNA backbone interactions that preserve DNA sequence specificity in adaptation of B3 domains to functional constraints associated with domain architecture.

Interaction Analysis between the Arabidopsis Transcription Repressor VAL1 and Transcription Coregulators SIN3-LIKEs (SNLs)

“…Since SNLs function as scaffold proteins in the SIN/HDAC complex, we speculate that SNLs may act as a bridge protein to connect the VAL1 and SIN/HDAC complex. VAL proteins can specifically bind the RY motif through their B3 domains in Arabidopsis and in rice [2,3,24,25]. In addition, numerous studies have revealed that the VAL (VAL1/2) proteins and the components of the SIN/HDAC complex, including SNLs, MSIs, HDA6, HDA19 and AtSAP18 proteins, are all involved in repression gene expression through mediating histone deacetylation in seed maturation and flowering transition [2,3,[6][7][8][9][11][12][13]23,[26][27][28][29][30][31][32][33][34].…”

LEAFY COTYLEDON 2: A Regulatory Factor of Plant Growth and Seed Development

“…LEC2 contains two domains named B2 and B3 [ 13 ]. It appears that the plant-specific B3 domain encoded by the LEC2 gene recognizes the conserved RY motif to transcriptionally regulate the expression of zygotic embryogenesis-specific genes and that it promotes somatic embryo formation at the maturation stage [ 12 , 14 , 15 ]. The LEC2 gene could be directly repressed by E2FA binding to an E2F-binding site during the seed maturation phase [ 16 ].…”