Functions of IQD proteins as hubs in cellular calcium and auxin signaling: A toolbox for shape formation and tissue-specification in plants?

Abstract

Calcium (Ca²⁺) ions play pivotal roles as second messengers in intracellular signal transduction, and coordinate many biological processes. Changes in intracellular Ca²⁺ levels are perceived by Ca²⁺ sensors such as calmodulin (CaM) and CaM-like (CML) proteins, which transduce Ca²⁺ signals into cellular responses by regulation of diverse target proteins. Insights into molecular functions of CaM targets are thus essential to understand the molecular and cellular basis of Ca²⁺ signaling. During the last decade, IQ67-domain (IQD) proteins emerged as the largest class of CaM targets in plants with mostly unknown functions. In the March issue of Plant Physiology, we presented the first comprehensive characterization of the 33-membered IQD family in Arabidopsis thaliana. We showed, by analysis of the subcellular localization of translational green fluorescent protein (GFP) fusion proteins, that most IQD members label microtubules (MTs), and additionally often localize to the cell nucleus or to membranes, where they recruit CaM Ca²⁺ sensors. Important functions at MTs are supported by altered MT organization and plant growth in IQD gain-of-function lines. Because IQD proteins share structural hallmarks of scaffold proteins, we propose roles of IQDs in the assembly of macromolecular complexes to orchestrate Ca²⁺ CaM signaling from membranes to the nucleus. Interestingly, expression of several IQDs is regulated by auxin, which suggests functions of IQDs as hubs in cellular auxin and calcium signaling to regulate plant growth and development.

Keywords: Auxin; IQD; KLCR/CMU; MP/ARF5; calcium; calmodulin; cell shape; microtubules.

Figure 1.

Model of IQD scaffolding function. (A) IQD proteins localize to the PM, MTs and cell nucleus, where they recruit CaM2 (and possibly other CaM/CML isoforms) as well as KLCR1/CMU1. Individual IQDs differentially affect MT organization and cell shape, which points to roles of plant-specific IQD families as a multifaceted toolbox for the regulation of cellular growth. ARF-mediated transcriptional control of IQD gene expression possibly links auxin and Ca²⁺ signaling. (B) IQD proteins share hallmarks of scaffold proteins, and interact with apo-CaM and Ca²⁺-CaM in vitro. We hypothesize that IQD proteins sequester apo-CaM and related Ca²⁺ sensors at distinct subcellular sites of Ca²⁺ influx to organize and integrate CaM/CML-dependent Ca²⁺ signaling.