Signaling and Communication in Plants
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1 Signaling and Communication in Plants Series Editors Frantisˇek Balusˇka Department of Plant Cell Biology, IZMB, University of Bonn, Kirschallee 1, D Bonn, Germany Jorge Vivanco Center for Rhizosphere Biology, Colorado State University, 217 Shepardson Building, Fort Collins, CO , USA For further volumes:
2 Shaul Yalovsky l František Baluška l Alan Jones Editors Integrated G Proteins Signaling in Plants
3 Editors Dr. Shaul Yalovsky Tel Aviv University Dept. Plant Sciences Ramat Aviv, Tel Aviv 603 Britannia Bldg. Israel Dr. František Baluška Department of Plant Cell Biology IZMB University of Bonn Kirschallee 1 D Bonn Germany baluska@uni-bonn.de Dr. Alan Jones University of North Carolina Dept. Biology & Pharmacology 317 Coker Hall Chapel Hill NC CB 3280 USA alan_jones@unc.edu ISSN: e-issn: ISBN: e-isbn: DOI / Springer Heidelberg Dordrecht London New York Library of Congress Control Number: # Springer-Verlag Berlin Heidelberg 2010 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer. Violations are liable to prosecution under the German Copyright Law. The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover design: WMXDesign GmbH, Heidelberg, Germany Printed on acid-free paper Springer is part of Springer Science+Business Media (
4 Preface When guanine nucleotide-binding proteins (G proteins) bind GTP, they adopt an activated conformation that leads to activation of downstream signaling elements. In this capacity, G proteins couple, amplify, and integrate upstream signals to downstream cellular changes. One of the most fascinating aspects of G proteins is that they operate like a molecular timer because the GTP-bound, activated state converts to the GDP-bound, resting state after an inherently determined amount of time due to hydrolysis of GTP to GDP by the intrinsic GTPase. The cycling of activated to resting states, known as the G cycle, enables cellular signaling to occur within kinetics of seconds to hours. In eukaryotes, G proteins are divided into two major subgroups: the Ras superfamily of small G proteins and the heterotrimeric G proteins. The Ras superfamily is further divided into the Ras, Rho, Rab, Arf, and Ran subfamilies. The Ga subunits of the heterotrimeric G-protein complex divide the complexes into four subclasses, G i,g s,g q, and G 12/13. The Ras, Rho, and the hetrotrimeric G proteins are implicated in regulation of signaling, while Rab, Arf, and Ran carry out other cellular functions and are not be covered in this book. Ras proteins have not been identified in plants. This leaves the small G protein from the Rho family, called ROPs or RACs (here after ROPs/RACs), and the heterotrimeric G proteins to comprise the two major groups of signaling G proteins in plants. This book summarizes a decade of research on ROPs/RACs and heterotrimeric G proteins in plants. In the active state, the small GTPases interact with target proteins commonly referred to as effectors to initiate a signaling process. In most small G proteins, the GDP/GTP exchange is not spontaneous and requires accessory proteins known as Gunanine nucleotide Exchange Factors (GEFs). The inefficient GTPase activity is enhance by a second group of proteins known as GTPase Activating Proteins (GAPs). GEFs and GAPs provide a means to regulate the activity of the small GTPases in time and space. Subcellular distribution of proteins from Rho and Rab families is regulated by a third group of proteins designated Guanine nucleotide Dissociation Inhibitors (GDIs). v
5 vi Preface Heterotrimeric G protein are composed of three subunits designated a, b, and g. The a subunit is a GTP-binding protein that contains one domain that resembles small GTPases. The b subunit has a seven-bladed propeller structure and forms a tight dimeric complex with the g subunit. In metazoans, heterotrimeric G proteins are associated with membrane proteins known as G-Protein-Coupled Receptors (GPCRs) that are the ligand-regulated GEFs. Activation of GPCRs upon ligand binding leads to GDP/GTP exchange and activation of the Ga. In turn, Gb- and Gg dissociate from the subunit as a complex and signaling is induced by both the dissociated Ga and Gb g complex. Signaling terminates by GTP hydrolysis that leads to reassociation of Gbg with the Ga. As discussed in the Chapter Bioinformatics of Seven-Transmembrane Receptors in Plant Genomes, the existence of GPCRs in plants is questioned. Furthermore, as discussed in the Chapter Plant Ga Structure and Properties, while GDP release from the Ga subunit is the rate-limiting step in vertebrate G protein complexes, that does not seem to be the case for Arabidopsis.The implications of this strange property are described. The book begins with a chapter from Janice Jones describing these and other G protein signaling principles and then describes the unique properties of plant heterotrimeric G proteins. The chapter Structure and function of ROPs and their GEFs, by ChristophThomas and Antje Berken takes a similar approach with the small G proteins and thus, these two chapters provide an interesting comparison of the Ga subunit of the heterotrimeric G protein complex and the small G proteins in plants. Physiological aspects are taken up in later chapters. For example, in the Chapter Heterotrimeric G Proteins and Plant Hormone Signaling in Rice, by Yukimoto Iwasaki and coworkers, evidence is presented that the G protein in rice is mediating fundamantally different signaling than in Arabidopsis. Jin-Gui Chen in the Chapter Heterotrimeric G-Proteins and Cell Division in Plants, builds the case that the heterotrimeric G protein complex controls the rate of the plant cell cycle and consequently cell proliferation. Two chapters ( The Role of Seven Transmembrane Domain MLO Proteins, Heterotrimeric G-Proteins and Monomeric RAC/ ROPs in Plant Defense and G Proteins and Plant Innate Immunity ) by Justine Lorek et al. and Yuri Trusov et al., respectively, deal with the role of small and heterotrimeric G proteins in plant defense against different pathogens. Whether or not G proteins couple multiple plant hormones and environmental signals remains an open question but is a theme throughout the book. As mentioned earlier, the receptors that activate the heterotrimeric G protein complex are poorly conserved at the primary sequence level. Therefore, in the Chapter Bioinformatics of Seven- Transmembrane Receptors in Plant Genomes, Etsuyko Moriyma and Stephen Opiyo provide strategies to identify 7-transmembrane proteins from divergent genomes. They then apply these tools to 18 genomes of the bikonts, the group that includes higher plants and the algae. The chapter Evolution of the ROP GTPase Signaling Module is about the bizaar; Lei Ding and coworkers discuss
6 Preface vii proteins that share limited sequence similarity to canonical Ga subunits of the heterotrimeric G protein complex. ROPs/RACs are master regulators of cell polarity, similar to their homologs in yeast and animal cells. Remarkably, these studies showed that regardless of the evolutionary-conserved functions, many of the ROPs/RACs effectors are unique to plants. The chapter ROP GTPases and the cytoskeleton by Ying Fu focuses on the function of ROPs/RACs in cytoskeleton organization, highlighting the role of a plant-unique group of proteins designated RICs (ROP Interacting CRIB containing) as well as by the evolutionary-conserved WAVE and Arp2/3 complexes. In the absence of other signaling small GTPases, ROPs/RACs were suggested to function in diverse signaling cascades. The chapter RAC/ROP GTPases in the Regulation of Polarity and Polar Cell Growth by He-Ming Wu and Alice Cheung describes the role of ROPs/RACs in cell polarity, hormonal, and reactive oxygen species signaling. The chapter highlights how conserved mechanisms involving proteins such as ADF/cofilins and formins together with plant-unique proteins such as the RICs and ICR1 (Interactor of Constitutive active ROP1) orchestrate polar cell growth. The chapter The Role of Seven Transmembrane Domain MLO Proteins, Heterotrimeric G-Proteins and Monomeric RAC/ROPs in Plant Defense by Justine Lorek et al. discusses the role of ROPs/RACs MLO proteins and hetrotrimeric G proteins in plant defense responses and how they interface with cell polarity, complementing the discussion in the chapter G proteins and plant innate immunity. Two types of ROP/RAC GEFs are currently known in plants: an evolutionary-conserved Dock180 protein called SPIKE1, which may be associated with the WAVE complex and a family of proteins designated PRONE GEFs that can activate ROPs/ RACs but not non-plant Rho proteins. In the chapter Structure and Function of ROPs and Their GEFs, Christoph Thomas and Antje Berken discuss the structure and function of ROPs/RACs and the PRONE ROPGEFs, highlighting the common and plant-unique features. GAPs and RhoGDIs play pivotal roles in regulation of signaling by Rho GTPases. The chapter Regulatory and Cellular Functions of Plant RhoGAPs and RhoGDIs by Benedikt Kost highlights studies showing how spatial distribution of certain GAPs and function of RhoGDIs regulate polar cell growth. The chapter Evolution of the ROP GTPase Signaling Module by John Fowler discusses the origin and evolution of ROPs/RACs. ROP/RACs and heterotrimeric G proteins function at the plasma membrane to which they attach by virtue of postranslational lipid modifications and polybasic region comprised of lysine and arginine residues. In the chapter Protein lipid Modifications and Targeting of ROP/RAC and Heterotrimeric G Proteins, Nadav Sorek and Shaul Yalovsky describe the lipid modifications and their regulatory roles in function of ROP/ RACs and heterotrimeric G proteins.each chapter of this book offers a different perspective of the state-of-the-art in the field, presenting a well-balanced and an upto-date description of the current knowledge on G protein signaling in plants. The breadth of the book offers a thourough introduction, and at the same time, a detailed in-depth discussion to those who are new to the field. Thus, we hope to draw the
7 viii Preface interest of both new and advanced students to this relatively young but fastprogressing and fascinating field of plant cell biology Tel Aviv, June 2009 Bonn, June 2009 Chapel Hill, June 2009 Shaul Yalovsky František Baluška Alan Jones
8 Contents Plant Ga Structure and Properties... 1 Janice C. Jones Regulatory and Cellular Functions of Plant RhoGAPs and RhoGDIs Benedikt Kost Structure and Function of ROPs and their GEFs Christoph Thomas and Antje Berken Protein Lipid Modifications and Targeting of ROP/RAC and Heterotrimeric G Proteins Nadav Sorek and Shaul Yalovsky ROP GTPases and the Cytoskeleton Ying Fu RAC/ROP GTPases in the Regulation of Polarity and Polar Cell Growth Hen-ming Wu, Christine Y. Chen, Qiaohong Duan, Daniel Kita, Candida Nibau, Li-zhen Tao, Yan-jiao Zou, and Alice Y. Cheung Heterotrimeric G Proteins and Plant Hormone Signaling in Rice Katsuyuki Oki, Yukiko Fujisawa, Hisaharu Kato, and Yukimoto Iwasaki Auxin, Brassinosteroids, and G-Protein Signaling Lei Wang and Kang Chong Heterotrimeric G-Proteins and Cell Division in Plants Jin-Gui Chen ix
9 x Contents Heterotrimeric G Protein Regulation of Stomatal Movements Sarah E. Nilson and Wei Zhang The Role of Seven-Transmembrane Domain MLO Proteins, Heterotrimeric G-Proteins, and Monomeric RAC/ROPs in Plant Defense Justine Lorek, Ralph Panstruga, and Ralph Hu ckelhoven G Proteins and Plant Innate Immunity Yuri Trusov, Lucı a Jorda, Antonio Molina, and Jose Ramon Botella Bioinformatics of Seven-Transmembrane Receptors in Plant Genomes Etsuko N. Moriyama and Stephen O. Opiyo Unconventional GTP-Binding Proteins in Plants Lei Ding, Timothy E. Gookin, and Sarah M. Assmann Evolution of the ROP GTPase Signaling Module John E. Fowler Index
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