Abstract
Signaling cross talks between auxin, a regulator of plant development, and Ca2+, a universal second messenger, have been proposed to modulate developmental plasticity in plants. However, the underlying molecular mechanisms are largely unknown. Here, we report that in Arabidopsis roots, auxin elicits specific Ca2+ signaling patterns that spatially coincide with the expression pattern of auxin-regulated genes. We have identified the single EF-hand Ca2+-binding protein Ca2+-dependent modulator of ICR1 (CMI1) as an interactor of the Rho of plants (ROP) effector interactor of constitutively active ROP (ICR1). CMI1 expression is directly up-regulated by auxin, whereas the loss of function of CMI1 associates with the repression of auxin-induced Ca2+ increases in the lateral root cap and vasculature, indicating that CMI1 represses early auxin responses. In agreement, cmi1 mutants display an increased auxin response including shorter primary roots, longer root hairs, longer hypocotyls, and altered lateral root formation. Binding to ICR1 affects subcellular localization of CMI1 and its function. The interaction between CMI1 and ICR1 is Ca2+-dependent and involves a conserved hydrophobic pocket in CMI1 and calmodulin binding-like domain in ICR1. Remarkably, CMI1 is monomeric in solution and in vitro changes its secondary structure at cellular resting Ca2+ concentrations ranging between 10−9 and 10−8 M. Hence, CMI1 is a Ca2+-dependent transducer of auxin-regulated gene expression, which can function in a cell-specific fashion at steady-state as well as at elevated cellular Ca2+ levels to regulate auxin responses.
Highlights
The plant hormone auxin regulates diverse developmental and physiological processes, serving as a morphogen that creates local maxima and gradients [1]
This long-term auxin accumulation is translated to gradients of transcription factors PLETHORA (PLT) genes and specific expression pattern of auxin response factors (ARFs) and their Aux/indole-3-acetic acid (IAA) inhibitors that have been shown to maintain the activity of root stem cells [5,6,7,8]
A typical auxin-induced Ca2+ signal was observed after 100 seconds of auxin (10 μM 1-Naphthaleneacetic acid [1Naphthaleneacetic acid (NAA)]) application and increased after 160 seconds (Fig 1A, “NAA 100 sec” and “160 sec”)
Summary
The plant hormone auxin regulates diverse developmental and physiological processes, serving as a morphogen that creates local maxima and gradients [1]. It is well documented that this accumulation happens early during embryo development and is essential for root meristem maintenance and root growth [1,2,3,4,5]. This long-term auxin accumulation is translated to gradients of transcription factors PLETHORA (PLT) genes and specific expression pattern of auxin response factors (ARFs) and their Aux/indole-3-acetic acid (IAA) inhibitors that have been shown to maintain the activity of root stem cells [5,6,7,8].
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