Plant Pumilio proteins: parallels and prospects of antagonistic functions in non-plant organisms

Pumilio (PUM) proteins belong to the Puf family of RNA binding proteins that shows very strong conservation across eukaryotes, both structurally and functionally. Their role in translational regulation is crucial in stem cell maintenance and embryonic development of eukaryotes. In numerous organisms, like humans, yeast, worms, and mice, Puf paralogs with very high sequence similarity exhibit opposing functions. Why and how this antagonism is established in plants remains unclear. Here, we present an overview of mechanisms of PUM function regulation observed in animals, and we draw parallels with the plant kingdom. We highlight mechanisms of selective association of PUM proteins with effector proteins, such as deadenylases or miRNAs, modifying their function from target mRNA-silencing to stabilization. Phosphorylation of PUMs can invert their molecular function from translation enhancer to repressor and vice versa . Moreover, different mRNA-binding modes confer structural changes in the backbone of the bound mRNA, which may attract different interactors, and enhance the binding specificity of the PUM protein itself. All these mechanisms can act in concert to establish functional antagonism of plant PUM proteins. We propose suitable experimental methods that can advance our understanding of the potential antagonistic functions of PUMs in plants. Overview of mechanisms that can lead to antagonistic functions of Puf family RNA binding proteins. Through facultative association with effector proteins, like the CCR4-NOT deadenylase, or association with miRNAs, PUMILIO (PUM) proteins can silence their target mRNAs or enhance translation depending on the physiological state. Likewise, condition-specific phosphorylation can alter protein structure and thereby change PUM’s affinity for their target mRNAs or effectors. Changes in mRNA binding modes can alter the target sequence and may provide opportunities for new effectors to bind. Finally, a combination of these mechanisms can broaden the roles of PUM proteins in the cell and allow for antagonistic functioning during development or in response to the environment. • PUMILIO RNA binding proteins are highly structurally and functionally conserved • In animals and fungi, PUMILIOs function antagonistically via different mechanisms • Comparing PUMILIOs in various eukaryotes provides new insights for plant biology • Emerging technologies and experimental approaches can contribute to identifying antagonistic functions of PUMILIOs in plants