Table Of ContentSignaling and Communication in Plants
Series Editors
FrantisˇekBalusˇka
DepartmentofPlantCellBiology,IZMB,UniversityofBonn,Kirschallee1,D-53115
Bonn, Germany
JorgeVivanco
CenterforRhizosphereBiology,ColoradoStateUniversity,217ShepardsonBuilding,
FortCollins, CO 80523-1173,USA
For furthervolumes:
http://www.springer.com/series/8094
Shaul Yalovsky Frantisˇek Balusˇka Alan Jones
l l
Editors
Integrated G Proteins
Signaling in Plants
Editors
Dr.ShaulYalovsky Dr.FrantisˇekBalusˇka
TelAvivUniversity DepartmentofPlantCellBiology
Dept.PlantSciences IZMB
69978RamatAviv,TelAviv UniversityofBonn
603BritanniaBldg. Kirschallee1
Israel D-53115Bonn
[email protected] Germany
[email protected]
Dr.AlanJones
UniversityofNorthCarolina
Dept.Biology&Pharmacology
317CokerHall
ChapelHillNC27599
CB3280
USA
[email protected]
ISSN:1867–9048 e-ISSN:1867–9056
ISBN:978-3-642-03523-4 e-ISBN:978-3-642-03524-1
DOI10.1007/978-3-642-03524-1
SpringerHeidelbergDordrechtLondonNewYork
LibraryofCongressControlNumber:2009934482
#Springer-VerlagBerlinHeidelberg2010
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Preface
When guanine nucleotide-binding proteins (G proteins) bind GTP, they adopt an
activatedconformationthatleadstoactivationofdownstream signaling elements.
In this capacity, G proteins couple, amplify, and integrate upstream signals to
downstreamcellularchanges.OneofthemostfascinatingaspectsofGproteinsis
that they operate like a molecular timer because the GTP-bound, activated state
convertstotheGDP-bound,restingstateafteraninherentlydeterminedamountof
time due to hydrolysis of GTP to GDP by the intrinsic GTPase. The cycling of
activatedtorestingstates,knownastheGcycle,enablescellularsignalingtooccur
withinkineticsofsecondstohours.Ineukaryotes,Gproteinsaredividedintotwo
majorsubgroups:theRassuperfamilyofsmallGproteinsandtheheterotrimericG
proteins. The Ras superfamily is further divided into the Ras, Rho, Rab, Arf, and
Ransubfamilies.TheGasubunits oftheheterotrimericG-proteincomplexdivide
the complexes into four subclasses, G, G, G , and G . The Ras, Rho, and the
i s q 12/13
hetrotrimericGproteinsareimplicatedinregulationofsignaling, whileRab,Arf,
andRancarryoutothercellularfunctionsandarenotbecoveredinthisbook.Ras
proteinshavenotbeenidentifiedinplants.ThisleavesthesmallGproteinfromthe
Rhofamily,calledROPsorRACs(hereafterROPs/RACs),andtheheterotrimeric
GproteinstocomprisethetwomajorgroupsofsignalingGproteinsinplants.This
book summarizes a decade of research on ROPs/RACs and heterotrimeric G
proteinsinplants.
In the active state, the small GTPases interact with target proteins commonly
referredtoaseffectorstoinitiateasignalingprocess.InmostsmallGproteins,the
GDP/GTP exchange is not spontaneous and requires accessory proteins known as
GunaninenucleotideExchangeFactors(GEFs).TheinefficientGTPaseactivityis
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
GTPasesintimeandspace.SubcellulardistributionofproteinsfromRhoandRab
families is regulated by a third group of proteins designated Guanine nucleotide
DissociationInhibitors(GDIs).
v
vi Preface
HeterotrimericGproteinarecomposedofthreesubunitsdesignateda,b,andg.
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
tightdimericcomplexwiththegsubunit.Inmetazoans,heterotrimericGproteins
are associated with membrane proteins known as G-Protein-Coupled Receptors
(GPCRs) that are the ligand-regulated GEFs. Activation of GPCRs upon ligand
bindingleadstoGDP/GTPexchangeandactivationoftheGa.Inturn,Gb-andGg
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
leadstoreassociationofGbgwiththeGa.AsdiscussedintheChapter“Bioinfor-
matics of Seven-Transmembrane Receptors in Plant Genomes,” the existence of
GPCRsinplantsisquestioned.
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
proteincomplexes,thatdoesnotseemtobethecaseforArabidopsis.Theimplica-
tionsofthisstrangepropertyaredescribed.
ThebookbeginswithachapterfromJaniceJonesdescribingtheseandotherG
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
smallGproteinsandthus,thesetwochaptersprovideaninterestingcomparisonof
theGasubunitoftheheterotrimericGproteincomplexandthesmallGproteinsin
plants. Physiological aspects are taken up in later chapters. For example, in the
Chapter “Heterotrimeric G Proteins and Plant Hormone Signaling in Rice,” by
YukimotoIwasakiandcoworkers,evidenceispresentedthattheGproteininriceis
mediating fundamantally different signaling than in Arabidopsis. Jin-Gui Chen in
theChapter“HeterotrimericG-ProteinsandCellDivisioninPlants,”buildsthecase
that the heterotrimeric G protein complex controls the rate of the plant cell cycle
andconsequentlycellproliferation.Twochapters(“TheRoleofSevenTransmem-
brane 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
heterotrimericGproteinsinplantdefenseagainstdifferentpathogens.Whetheror
notGproteinscouplemultipleplanthormonesandenvironmentalsignalsremains
an open question but is a theme throughout the book. As mentioned earlier, the
receptorsthatactivatetheheterotrimericGproteincomplexarepoorlyconservedat
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
Preface vii
proteins that share limited sequence similarity to canonical Ga subunits of the
heterotrimericGproteincomplex.
ROPs/RACs aremasterregulators ofcell polarity, similartotheir homologsin
yeast and animal cells. Remarkably, these studies showed that regardless of the
evolutionary-conservedfunctions,manyoftheROPs/RACseffectorsareuniqueto
plants.Thechapter“ROPGTPasesandthecytoskeleton”byYingFufocusesonthe
function of ROPs/RACs in cytoskeleton organization, highlighting the role of a
plant-uniquegroupofproteinsdesignatedRICs(ROPInteractingCRIBcontaining)
as well as by the evolutionary-conserved WAVE and Arp2/3 complexes. In the
absenceofothersignalingsmallGTPases,ROPs/RACsweresuggestedtofunction
indiversesignalingcascades.Thechapter“RAC/ROPGTPasesintheRegulation
ofPolarityandPolarCellGrowth“byHe-MingWuandAliceCheungdescribesthe
roleofROPs/RACsincellpolarity,hormonal,andreactiveoxygenspeciessignal-
ing.Thechapterhighlightshowconservedmechanismsinvolvingproteinssuchas
ADF/cofilinsandforminstogetherwithplant-uniqueproteinssuchastheRICsand
ICR1 (Interactor of Constitutive active ROP1) orchestrate polar cell growth. The
chapter “The Role of Seven Transmembrane Domain MLO Proteins, Heterotri-
meric G-Proteins and Monomeric RAC/ROPs in Plant Defense” by Justine Lorek
etal.discussestheroleofROPs/RACsMLOproteinsandhetrotrimericGproteins
inplantdefenseresponsesandhowtheyinterfacewithcellpolarity,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 com-
plex 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
ROPsandTheirGEFs,”ChristophThomasandAntjeBerkendiscussthestructure
andfunctionofROPs/RACsandthePRONEROPGEFs,highlightingthecommon
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 RhoGAPsand 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
FowlerdiscussestheoriginandevolutionofROPs/RACs.ROP/RACsandhetero-
trimericGproteinsfunctionattheplasmamembranetowhichtheyattachbyvirtue
ofpostranslationallipidmodificationsandpolybasicregioncomprisedoflysineand
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
perspectiveofthestate-of-the-artinthefield,presentingawell-balancedandanup-
to-datedescriptionofthecurrentknowledgeonGproteinsignalinginplants.The
breadthofthebookoffersathouroughintroduction,andatthesametime,adetailed
in-depth discussion to those who are new to the field. Thus, we hope to draw the
viii Preface
interest of both new and advanced students to this relatively young but fast-
progressingandfascinatingfieldofplantcellbiology
TelAviv,June2009 ShaulYalovsky
Bonn,June2009 FrantisˇekBalusˇka
ChapelHill,June2009 AlanJones
Contents
PlantGaStructureandProperties ........................................... 1
Janice C. Jones
RegulatoryandCellularFunctionsofPlantRhoGAPs
andRhoGDIs ................................................................ 27
Benedikt Kost
StructureandFunctionofROPsandtheirGEFs ........................... 49
Christoph Thomas and Antje Berken
Protein–LipidModificationsandTargetingofROP/RAC
andHeterotrimericGProteins .............................................. 71
Nadav Sorek and Shaul Yalovsky
ROPGTPasesandtheCytoskeleton ........................................ 91
Ying Fu
RAC/ROPGTPasesintheRegulationofPolarity
andPolarCellGrowth ...................................................... 105
Hen-mingWu,ChristineY.Chen,QiaohongDuan,DanielKita,
CandidaNibau,Li-zhenTao,Yan-jiaoZou,andAliceY.Cheung
HeterotrimericGProteinsandPlantHormoneSignalinginRice .......... 123
KatsuyukiOki,YukikoFujisawa,HisaharuKato,
andYukimotoIwasaki
Auxin,Brassinosteroids,andG-ProteinSignaling .......................... 135
Lei Wang and Kang Chong
HeterotrimericG-ProteinsandCellDivisioninPlants ..................... 155
Jin-Gui Chen
ix
x Contents
HeterotrimericGProteinRegulationofStomatalMovements ............. 177
Sarah E. Nilson and Wei Zhang
TheRoleofSeven-TransmembraneDomainMLOProteins,
HeterotrimericG-Proteins,andMonomericRAC/ROPs
inPlantDefense ............................................................ 197
Justine Lorek, Ralph Panstruga, and Ralph Hu¨ckelhoven
GProteinsandPlantInnateImmunity ..................................... 221
Yuri Trusov, Lucı´a Jorda´, Antonio Molina, and Jose Ramon Botella
BioinformaticsofSeven-TransmembraneReceptors
inPlantGenomes ........................................................... 251
Etsuko N. Moriyama and Stephen O. Opiyo
UnconventionalGTP-BindingProteinsinPlants ........................... 279
LeiDing,TimothyE.Gookin,andSarahM.Assmann
EvolutionoftheROPGTPaseSignalingModule .......................... 305
JohnE.Fowler
Index ........................................................................ 329
Plant Ga Structure and Properties
JaniceC.Jones
Abstract G-protein-coupled receptors (GPCRs) are a large family of eukaryotic
membrane-spanning proteins that convert signals from the outside of a cell to an
appropriate response inside the cell. GPCRs typically associate with a heterotri-
meric Gabg protein. Activated receptors propagate signals by causing the Ga
subunit of the heterotrimer to release GDP and to bind GTP. GTP binding causes
a conformational change in the Ga protein that triggers heterotrimer dissociation
anddownstreamsignaling.Inthisway,theguaninenucleotideoccupancyoftheGa
subunit determines the protein structure and activity. Although most of the G
protein paradigm has been established by studying animal G proteins, recent
researchhasrevealeddiverserolesforGproteinsignalinginplants.Thefirstpart
of the chapter (Section “Introduction: Structure-Function Relationships in G Pro-
teinSignaling”inChapter“PlantGaStructureandProperties”)reviewsGprotein
signaling principles, with an emphasis on the information that has been gleaned
fromatomicstructures.Thesecondpart(Section“ComparisonofPlantGaProteins
to Mammalian Ga Proteins” in Chapter, “Plant Ga Structure and Properties”)
compares plant Ga proteins to animal Ga proteins with an emphasis on how
structureconfersfunctionfortheseproteins.AlthoughplantandanimalGaproteins
share less than 40% identity, the key residues that confer G protein function are
nearlyinvariantacrossallGproteinfamilies.Thethirdpart(Section“Propertiesof
Plant Ga Proteins” in Chapter “Plant Ga Structure and Properties”) describes the
physicalpropertiesofplantGaproteins,includingkineticproperties,localization,
receptorcoupling,andeffectoractivation.
J.C.Jones
DivisionofBiochemistryandBiophysics,DepartmentofBiology,UniversityofNorthCarolina,
POBox7260,ChapelHill,NC27599,USA
e-mail:[email protected]
S.Yalovskyetal.(eds.),IntegratedGProteinsSignalinginPlants, 1
SignalingandCommunicationinPlants,
DOI10.1007/978-3-642-03524-1_1,#Springer-VerlagBerlinHeidelberg2010
