It's Morphin' time: how multiple signals converge on ARF transcription factors to direct development

Abstract

Plant development programs are constantly updated by information about environmental conditions, currently available resources, and sites of active organogenesis. Much of this information is encoded in modifications of transcription factors that lead to changes in their relative abundance, activity and localization. Recent work on the Auxin Response Factor family of transcription factors has highlighted the large diversity of such modifications, as well as how they may work synergistically or antagonistically to regulate downstream responses. ARFs can be regulated by alternative splicing, post-translational modification, and subcellular localization, among many other mechanisms. Beyond the many ways ARFs themselves can be regulated, they can also act cooperatively with other transcription factors to enable highly complex genetic networks with distinct developmental outcomes. Multi-level regulation like what has been documented for ARFs has the capacity to generate flexibility in transcriptional outputs, as well as resilience to short-term perturbations.

Figure 1:. Regulation of ARF function at the transcriptional and protein level.

A. Different ARFs show spatially specific expression patterns, as exemplified by the pattern of class A ARF expression in the root. Likely cis-elements within the unique ARF promoters and the first intron regulate tissue-specific expression. B. Alternative splicing can regulate ARF expression profiles and function—a splice variant of ARF8, ARF8.4, is only expressed in developing flowers. This variant binds more strongly to regions of the IAA19 promoter that include G-boxes and HUD-box elements, potentially by interacting with bHLH or other transcription factors that bind to these elements. The more globally expressed variant ARF8.1 binds less strongly to this promoter, potentially because its protein structure disallows binding to interaction partners. C. ARF protein localization is regulated on the subcellular level—ARF7 and ARF19 localize to the nucleus in the meristematic region of the primary root, where they promote transcription of auxin target genes, but aggregate in the cytoplasm in the differentiation zone, where they are no longer active.

Figure 2:. Post-translational regulation of ARF activity.

ARF activity is regulated by phosphorylation and sumoylation. A. Phosphorylation of the B class ARF2 by GSK3 kinase BIN2 decreases its affinity for DNA, potentially decreasing competition for binding sites and allowing A class ARFs to bind promoters and activate transcription. B. Phosphorylation of ARF7 and ARF19 by BIN2 promotes transcription by interfering with the interacting between ARF7 and its repressor IAA proteins. C. Sumoylation of ARF7 promotes the interaction between ARF7 and the IAA3 repressor and decreases ARF DNA-binding affinity. Removal of the SUMO group by proteases OTS1/OTS2 decreases the strength of IAA3-ARF7 interactions and increases ARF7 binding to and activity on the promoters of target genes.