calmodulina - proteinas

  • Published on
    01-Dec-2014

  • View
    48

  • Download
    2

Embed Size (px)

Transcript

Plant-Specic Calmodulin-Binding ProteinsAnnu. Rev. Plant Biol. 2005.56:435-466. Downloaded from arjournals.annualreviews.org by Universidade Federal Rural da Amazonia on 03/03/10. For personal use only.

Nicolas Bouch ,1 Ayelet Yellin,2 e Wayne A. Snedden,3 and Hillel Fromm21

Institut National de la Recherche Agronomique, Institut Jean-Pierre Bourgin, Laboratoire de Biologie Cellulaire, 78026 Versailles, France; email: bouche@versailles.inra.fr Department of Plant Sciences, Tel Aviv University, Tel Aviv, 69978 Israel; email: yellinay@post.tau.ac.il, hillelf@post.tau.ac.il Department of Biology, Queens University, Kingston, Ontario, K7L 3N6, Canada; email: sneddenw@biology.queensu.ca

2

3

Annu. Rev. Plant Biol. 2005. 56:43566 doi: 10.1146/ annurev.arplant.56.032604.144224 Copyright c 2005 by Annual Reviews. All rights reserved First published online as a Review in Advance on January 18, 2005 1543-5008/05/06020435$20.00

Key Wordscalcium, signal transduction, environmental stress, Arabidopsis

AbstractCalmodulin (CaM) is the most prominent Ca2+ transducer in eukaryotic cells, regulating the activity of numerous proteins with diverse cellular functions. Many features of CaM and its downstream targets are similar in plants and other eukaryotes. However, plants possess a unique set of CaM-related proteins, and several unique CaM target proteins. This review discusses recent progress in identifying plant-specic CaMbinding proteins and their roles in response to biotic and abiotic stresses and development. The review also addresses aspects emerging from recent structural studies of CaM interactions with target proteins relevant to plants.

435

ContentsINTRODUCTION: THE LANGUAGE OF CALCIUM SIGNALING . . . . . . . . . . . . . . . . . . . . . 436 Ca2+ as a Signal Carrier in Living Organisms . . . . . . . . . . . . . . . . . . . . . . 436 Ca2+ -Modulated Proteins in Plants . 437 CALMODULIN-TARGET INTERACTIONS . . . . . . . . . . . . . . . . 439 Structural Analysis and Functional Implications . . . . . . . . . . . . . . . . . . . . 439 The Repertoire of CaM Target Proteins in Plants . . . . . . . . . . . . . . . 441 CALMODULIN AND PLANT RESPONSE TO ABIOTIC STRESS . . . . . . . . . . . . . . . . . . . . . . . . . . 443 Response to Osmotic Stress and Salinity . . . . . . . . . . . . . . . . . . . . . . . . . 444 Response to Cold and Heat Stresses . . . . . . . . . . . . . . . . . . . . . . . . .445 CaMBPs and Oxidative Stress . . . . . . 446 Activation of Glutamate Decarboxylase by Environmental Stresses and Production of GABA . . . . . . . . . . . . 447 Tolerance to Xenobiotic Compounds . . . . . . . . . . . . . . . . . . . . 448 CALMODULIN AND PLANT RESPONSE TO BIOTIC STRESS . . . . . . . . . . . . . . . . . . . . . . . . . . 449 CaMs and CMLs in Pathogen Response . . . . . . . . . . . . . . . . . . . . . . . 449 CaM Targets and Pathogen Response . . . . . . . . . . . . . . . . . . . . . . . 451 CALMODULIN AND PLANT DEVELOPMENT . . . . . . . . . . . . . . . . 453 CaMBPs Responding to Hormonal Treatment . . . . . . . . . . . . . . . . . . . . . . 453 CaM and CaMBPs Involved in the Development of Polarized Cells. . . . . . . . . . . . . . . . . .454 CONCLUDING REMARKS AND FUTURE DIRECTIONS . . . . . . . . . 456

INTRODUCTION: THE LANGUAGE OF CALCIUM SIGNALING Ca2+ as a Signal Carrier in Living OrganismsAll organisms continually monitor their environment and respond to changes with adaptive mechanisms that are initiated at the molecular and biochemical levels and require the coordination of cellular events to ensure that a response is appropriate for a given stimulus. Therefore, complex intra- and intercellular communication networks have evolved to convey information about a perceived stimulus to the cellular machinery responsible for mediating the responses. Organisms use various small organic and inorganic molecules, termed second messengers (e.g., Ca2+ , cyclic nucleotides, phospholipids, sugars, amino acids), to encode information and deliver it to downstream effectors, which decode signals and initiate cellular responses including changes in enzyme activity, gene expression, transport across membranes, and cytoskeletal rearrangement. Ca2+ is one of the most prominent second messengers in eukaryotes, and its roles as a signal carrier are the subject of intensive investigations in both animals and plants. The reader is also referred to more specic reviews on different aspects of Ca2+ signaling in plants (73, 76, 145, 174). In recent years, there has been a major effort directed toward elucidating the information carried in the Ca2+ signals evoked by exogenous stimuli. Spatial and temporal propagation of the Ca2+ signals, the amplitude of the signal, which is typically proportional to the strength of the stimulus, and the frequency of oscillations are all elements of information carried by the Ca2+ signal that must be decoded by the cellular machinery. Spatial distribution of the Ca2+ signal in the cell is controlled by a complex network of Ca2+ -permeable channels, Ca2+ -antiporters, and Ca2+ -pumps, which operate at the plasma membrane or in membranes of intracellular Ca2+ stores including the ER, mitochondria, chloroplast, and the vacuole,

Annu. Rev. Plant Biol. 2005.56:435-466. Downloaded from arjournals.annualreviews.org by Universidade Federal Rural da Amazonia on 03/03/10. For personal use only.

436

Bouch et al. e

and are regulated by different second messengers (reviewed in 76). Of particular interest is the relationship between cytosolic and nuclear Ca2+ . Ca2+ signals in the cytosol and in the nucleus have distinct functions in both animals (13, 18, 71) and plants (169). Recent investigations (13, 132) suggest that although nuclear Ca2+ signals in many cases reect the patterns of cytosolic Ca2+ , the nucleus can also generate stimulus-induced signals independently. There is evidence that the nucleus contains intrinsic Ca2+ signaling machinery that can release Ca2+ locally in discrete nuclear regions. Echevarra et al. (54) identied a nucleoplasmic reticulum in epithelial cells, composing a branching intranuclear network continuous with the nuclear envelope and the endoplasmic reticulum. These structures function as a nuclear Ca2+ -storing network that can give rise to localized Ca2+ gradients and thus Ca2+ -dependent events can be regulated differentially in the nucleus, just as they are in the cytosol. It is likely that plants possess similar intranuclear Ca2+ stores. One important question concerning the role of Ca2+ as a second messenger is how cells control stimulus-response specicity. There is evidence that the frequency of Ca2+ oscillations carries information that is decoded by cellular targets in both plants and animals. In plants this was elegantly demonstrated by studying the Arabidopsis det3 mutant, which is unable to close its stomata in response to exogenous Ca2+ . However, stomatal closure could be restored in det3 by subjecting it to articial Ca2+ oscillations (4). Changes in the frequency or duration of the Ca2+ oscillations inuenced stomatal aperture. These studies indicate a specic mechanism to translate Ca2+ signals into a cellular response (3, 5). The nature of these decoders is intriguing. One can speculate that decoding Ca2+ signals requires proteins that can respond to Ca2+ oscillations by ne conformational changes. De Koninck & Schulman (44) found that the CaM-dependent protein KinaseII is sensitive to the frequency of Ca2+ oscillations in vitro in a way that is reected in the autonomous kinase activity, suggesting that

Annu. Rev. Plant Biol. 2005.56:435-466. Downloaded from arjournals.annualreviews.org by Universidade Federal Rural da Amazonia on 03/03/10. For personal use only.

CaMKII is a decoder of the frequency of Ca2+ oscillations. Other studies showed that oscillations increase both the efcacy and information content of Ca2+ signals that lead to gene expression and cell differentiation (50). Certain transcription factors are activated only by highfrequency Ca2+ oscillations, whereas others may be activated by infrequent oscillations (50) or both high-frequency and low-frequency oscillations. A recent review addressed the role of plant protein kinases in decoding Ca2+ signals (73). Given the importance of Ca2+ -modulated proteins in decoding Ca2+ signals, it is important to consider the repertoire of plant Ca2+ modulated proteins.

ER: endoplasmic reticulum CaM: calmodulin Calmodulin: CaM is a ubiquitous Ca2+ sensor protein (16 to 18 kD) with no catalytic activity that can, upon binding Ca2+ , activate target proteins involved in various cellular processes. The CaM prototype is comprised of two globular domains connected with a long exible helix. Each globular domain contains a pair of intimately linked EF hands. One EF hand motif is composed of a specialized helix-loop-helix structure that binds one molecule of Ca2+ .

Ca2+ -Modulated Proteins in PlantsMost proteins that function as transducers of Ca2+ signals contain a common structural motif, the EF hand (125), which is a helix-loophelix structure that binds a single Ca2+ ion. These motifs typically, but not exclusively, occur in closely linked pairs, interacting through antiparallel -sheets (125). This arrangement is the basis for cooperativity in Ca2+ binding. The superfamily of EF-hand proteins is divided into several classes based on differences in number and organization of EF-hand pairs, amino acid sequences within or outside the motifs, afnity to Ca2+ , and/or selectivity and afnity to target proteins (39, 125). Nakayama et al. (124) discussed the evolution of EF-hand proteins and divided them into 66 subfamilies. Day et al. (42) reported a comprehensive bioinformatic search for EF-hand-containing proteins in Arabidopsis. Other reviews discuss specic families of EF-hand proteins in