A novel Ca2+-binding protein that can rapidly transduce auxin responses during root growth

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...

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Published in:	PLoS biology Vol. 17; no. 7; p. e3000085
Main Authors:	Hazak, Ora, Mamon, Elad, Lavy, Meirav, Sternberg, Hasana, Behera, Smrutisanjita, Schmitz-Thom, Ina, Bloch, Daria, Dementiev, Olga, Gutman, Itay, Danziger, Tomer, Schwarz, Netanel, Abuzeineh, Anas, Mockaitis, Keithanne, Estelle, Mark, Hirsch, Joel A, Kudla, Jörg, Yalovsky, Shaul
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 11-07-2019 Public Library of Science (PLoS)
Subjects:	Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Auxin Binding sites Biology Biology and Life Sciences Biotechnology Calcium - metabolism Calcium ions Calcium signalling Calcium-binding protein Calcium-binding proteins Calcium-Binding Proteins - genetics Calcium-Binding Proteins - metabolism Calmodulin Carrier Proteins - genetics Carrier Proteins - metabolism Cellular structure Developmental plasticity EF-hand Food security Funding Gene expression Gene Expression Profiling - methods Gene Expression Regulation, Developmental - drug effects Gene Expression Regulation, Developmental - genetics Gene Expression Regulation, Plant - drug effects Gene Expression Regulation, Plant - genetics Growth Hydrophobicity Hypocotyls Indoleacetic Acids - metabolism Indoleacetic Acids - pharmacology Kinases Localization Molecular modelling Mutants Nitrates Peptides Physiological aspects Plant Roots - genetics Plant Roots - growth & development Plant Roots - metabolism Plant sciences Plants, Genetically Modified Protein Binding Protein structure Proteins Research and Analysis Methods Root hairs Roots Roots (Botany) Secondary structure Signal Transduction - drug effects Signal Transduction - genetics Signaling Supervision Israel California Indiana Tel Aviv Israel United States > US Germany
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Summary:	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.
Bibliography:	new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Biology, University of Fribourg, Switzerland. Current address: Division of Biological Sciences, University of California San Diego, San Diego, California, United States of America. The authors have declared that no competing interests exist. Current address: CSIR-Indian Institute of Chemical Biology, Kolkata, India.
ISSN:	1545-7885 1544-9173 1545-7885
DOI:	10.1371/journal.pbio.3000085