VOLU METHREEHUNDREDANDTWENTYSIX I R NTERNATIONAL EVIEW OF CELL AND MOLECULAR BIOLOGY International Review of Cell and Molecular Biology SeriesEditors GEOFFREYH.BOURNE 1949—1988 JAMESF.DANIELLI 1949—1984 KWANGW.JEON 1967— MARTINFRIEDLANDER 1984—1992 JONATHANJARVIK 1993—1995 LORENZOGALLUZZI 2016— EditorialAdvisoryBoard PETERL.BEECH BRUCED.MCKEE ROBERTA.BLOODGOOD MICHAELMELKONIAN BARRYD.BRUCE KEITHE.MOSTOV DAVIDM.BRYANT ANDREASOKSCHE KEITHBURRIDGE MADDYPARSONS HIROOFUKUDA TERUOSHIMMEN MAYGRIFFITH ALEXEYTOMILIN KEITHLATHAM GARYM.WESSEL WALLACEF.MARSHALL VOLU METHREEHUNDREDANDTWENTYSIX I R NTERNATIONAL EVIEW OF CELL AND MOLECULAR BIOLOGY Editedby KWANG W. JEON DepartmentofBiochemistry UniversityofTennessee Knoxville,Tennessee LORENZO GALLUZZI DepartmentofRadiation Oncology WeillCornellMedical College NewYork,New York AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON NEWYORK(cid:129)OXFORD(cid:129)PARIS(cid:129)SANDIEGO SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO AcademicPressisanimprintofElsevier AcademicPressisanimprintofElsevier 125LondonWall,LondonEC2Y5AS,UK 525BStreet,Suite1800,SanDiego,CA92101-4495,USA 50HampshireStreet,5thFloor,Cambridge,MA02139,USA TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK Firstedition2016 Copyright©2016ElsevierInc.AllRightsReserved. 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ISBN:978-0-12-804805-4 ISSN:1937-6448 ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/ Publisher:ZoeKruze AcquisitionEditor:AlexWhite EditorialProjectManager:HeleneKabes ProductionProjectManager:MageshKumarMahalingam Designer:MatthewLimbert TypesetbyThomsonDigital CONTRIBUTORS M.HajiAbdolvahab DepartmentofPharmaceutics,UtrechtInstituteforPharmaceuticalSciences(UIPS), UtrechtUniversity,Utrecht,Netherlands A.W.R.Arokiaraj SchoolofBiologicalSciences,UniversityofHongKong,HongKong,China A.-S.Bohrer DepartmentofBiochemistryandMolecularBiology,MichiganStateUniversity, EastLansing,MI,UnitedStates Y.Chen SchoolofBiomedicalSciences,FacultyofMedicine,ChineseUniversityofHongKong, Shatin,NewTerritories,HongKong;StateKeyLaboratoryofDigestiveDisease,Instituteof DigestiveDisease,ChineseUniversityofHongKong,Shatin,NewTerritories,HongKong; ShenzhenResearchInstitute,ChineseUniversityofHongKong,Shenzhen,China B.K.C.Chow SchoolofBiologicalSciences,UniversityofHongKong,HongKong,China G.DeRossi WilliamHarveyResearchInstitute,BartsandLondonSchoolofMedicineandDentistry, QueenMaryCollege,UniversityofLondon,London,UnitedKingdom P.Fonseca DepartmentofOncology-Pathology,KarolinskaInstitutetandUniversityHospital, Stockholm,Sweden J.M.P.Freije DepartmentofBiochemistryandMolecularBiology,SchoolofMedicine, UniversityofOviedo,Oviedo,Spain K.Kikuchi DevelopmentalandStemCellBiologyDivision,VictorChangCardiacResearchInstitute, Darlinghurst;St.Vincent’sClinicalSchool,UniversityofNewSouthWales,Kensington, NSW,Australia C.Lo´pez-Ot´ın DepartmentofBiochemistryandMolecularBiology,SchoolofMedicine,Universityof Oviedo,Oviedo,Spain ix x Contributors C.H.Li SchoolofBiomedicalSciences,FacultyofMedicine,ChineseUniversityofHongKong, Shatin,NewTerritories,HongKong,China M.R.K.Mofrad MolecularCellBiomechanicsLaboratory,DepartmentsofBioengineeringandMechanical Engineering,UniversityofCalifornia,Berkeley,CA,UnitedStates A.Occhionero DepartmentofOncology-Pathology,KarolinskaInstitutetandUniversityHospital, Stockholm,Sweden F.G.Osorio DepartmentofBiochemistryandMolecularBiology,SchoolofMedicine, UniversityofOviedo,Oviedo,Spain T.Panaretakis DepartmentofOncology-Pathology,KarolinskaInstitutetandUniversityHospital, Stockholm,Sweden O.Santiago-Ferna´ndez DepartmentofBiochemistryandMolecularBiology,SchoolofMedicine, UniversityofOviedo,Oviedo,Spain H.Schellekens DepartmentofPharmaceutics,UtrechtInstituteforPharmaceuticalSciences(UIPS), UtrechtUniversity,Utrecht,Netherlands R.Sekar SchoolofBiologicalSciences,UniversityofHongKong,HongKong,China K.Singh SchoolofBiologicalSciences,UniversityofHongKong,HongKong,China C.Soria-Valles DepartmentofBiochemistryandMolecularBiology,SchoolofMedicine, UniversityofOviedo,Oviedo,Spain H.Takahashi DepartmentofBiochemistryandMolecularBiology,MichiganStateUniversity,East Lansing,MI,UnitedStates I.Vardaki DepartmentofOncology-Pathology,KarolinskaInstitutetandUniversityHospital, Stockholm,Sweden J.R.Whiteford WilliamHarveyResearchInstitute,BartsandLondonSchoolofMedicineandDentistry, QueenMaryCollege,UniversityofLondon,London,UnitedKingdom Contributors xi A.Woodfin CardiovascularDivision,King’sCollege,UniversityofLondon,London,UnitedKingdom M.S.W.Xiang DevelopmentalandStemCellBiologyDivision,VictorChangCardiacResearchInstitute, Darlinghurst,NSW,Australia CHAPTERONE Compartmentalization and Regulation of Sulfate Assimilation Pathways in Plants A.-S.Bohrer,H.Takahashi* DepartmentofBiochemistryandMolecularBiology,MichiganStateUniversity,EastLansing,MI,UnitedStates *Correspondingauthor.E-mailaddress:[email protected] Contents 1. Introduction 2 2. SulfateTransportSystems 3 2.1 MolecularCloningofSulfateTransporter 3 2.2 SulfateUptakeinRoots 4 2.3 SulfateDistributioninPlants 9 3. SulfateAssimilation 16 3.1 MetabolicPathwayCompartmentalizationandRegulation 16 3.2 Plastid-CytosolMetabolicPathwayIntegration 20 4. ConclusionsandFuturePerspectives 23 Acknowledgments 25 References 25 Abstract Plants utilize sulfate to synthesize primary and secondary sulfur-containing metabo- litesrequiredforgrowthandsurvivalintheenvironment.Sulfateistakenupintoroots fromthesoilanddistributedtovariousorgansthroughthefunctionsofmembrane- boundsulfatetransporters,whileitisutilizedastheprimarysubstrateforsynthesizing sulfur-containing metabolites in the sulfate assimilation pathways. Transporters and enzymesfor the assimilativeconversion of sulfateare regulatedin highlyorganized mannersdependingonchangesinsulfatesupplyfromtheenvironmentanddemand forbiosynthesisofreducedsulfurcompoundsintheplantsystems.Overthepastfew decades,theeffectofsulfurnutritionongeneexpressionofsulfatetransportersand assimilatoryenzymeshasbeenextensivelystudiedwiththeaimofunderstandingthe fulllandscapeofregulatorynetworks. InternationalReviewofCellandMolecularBiology,Volume326 ISSN1937- 6448 ©2016ElsevierInc. http:/ /dx.doi.org /10.1016/bs.ircmb.2016.03.001 A llrig htsreser ved. 1 2 A.-S.BohrerandH.Takahashi 1. INTRODUCTION Sulfur is an essential macronutrient required for the growth and development of all living organisms. Sulfur is present in a wide variety of metabolites important for the maintenance of cell structure and biological activities(Leusteketal.,2000;Takahashietal.,2011).Inthesulfurcyclein nature, plants as producers and soil microorganisms as decomposers use distinct types of substrates in assimilative and dissimilative pathways of sulfur m etabo lism (Takahas hi et al., 2011) . Pla nts utilize su lfate (SO2 (cid:1)), 4 themostoxidizedinorganicformofsulfurforsynthesizingsulfur-contain- ing metabolites (Leustek et al., 2000; Takahashi et al., 2011). In this assi milative path way, plan ts redu ce sulf ate (SO2(cid:1)) to sulf ide (S2(cid:1) ) u sing 4 the energy derived from photosynthesis. Sulfide is subsequently used for synthesizing cysteine and other organic sulfur compounds in the down- stream metabolic pathways. In contrast, soil microorganisms can decom- posesulfatedandsulfonatedcompoundsfromwastesandremainsofplants and animals, and mineralize them to sulfate through the dissimilative oxidation pathway. Sulfur is also cycled in the atmosphere and the aquatic environment. Plants grow in the environment where the availability of sulfur source may change due to climate conditions and other biological and anthropo- genic factors affecting the fluxes of the sulfur cycle. They also experience extreme changes in the environment where production of antioxidants may become crucially important for alleviating the oxidative stresses. Furthermore,plantsareoftenbeingchallengedbypathogensandherbivores. Sinceplantsgrowunder theseadverseenvironmentalconditions,theyhave rationalstrategiestomodulatetheactivityofsulfateassimilationandtoutilize sulfur-containing metabolites to mitigate the stresses. Gene expression and activityofsulfatetransportersandsulfateassimilatoryenzymesarecontrolled inresponsetochangesinsulfatesupplyanddemandfor sulfuratthewhole plantlevel.Sulfur-containingphytoalexins,suchasglucosinolatesandcama- lexins, are synthesized to be used as chemical protectants against pathogens (HalkierandGershenzon,2006;Glawischnig,2007).Thetripeptidegluta- thione(GSH) isessentialfor removalof reactiveoxygenspecies(Foyerand Noctor,2009).PhytochelatinsderivedfromGSHsequesterheavymetalsas metal-thiolateconjugates(Zenk,1996).Sulfurinallthesesulfur-containing metabolites derives from sulfate acquired from the environment. This pro- videsanimplicationthatalteringtheamountofsulfur inputor modulating CompartmentalizationandRegulationofSulfateAssimilationPathwaysinPlants 3 thefluxofinternalsulfurutilizationcaneitherenhanceorlimitthebiological activityofplantsinnature. Molecular mechanisms of sulfate uptake and assimilation have been extensively studied over the past few decades. Precise documentations of biochemical properties, spatial localization, and conditional regulation of sulfatetransportersandmetabolicenzymeshaveextendedourunderstanding of this metabolic pathway in plants. Findings of regulatory components (genes, RNAs, and proteins) for transcriptional and posttranscriptional mechanismshaveprovideduswithcluestoinvestigatetheregulatorypath- ways. Recent studies provide evidence that these regulatory components control sulfate uptake and metabolism in a highly organized manner. This reviewarticleprovidesupdatedinformationonsulfatetransportandassim- ilationpathwaysinplantswithaparticularfocusontheircompartmentalized functionsandmolecularmechanismsofregulationdemonstratedinamodel plantspeciesArabidopsisthaliana. 2. SULFATE TRANSPORT SYSTEMS 2.1 Molecular Cloning of Sulfate Transporter Theexistenceofcarrier-mediatedsulfatetransportsystemsinplantrootshas been suggested from the results of sulfate uptake measurements in physio- logical studies dating back to the 1950s (Leggett and Epstein, 1956). However, the identification of plant genes encoding sulfate transporters was reported years later based on a molecular biological approach using a yeast mutant as a heterologous expression system for cDNA cloning (Smithetal.,1995a).Theyeastmutantslackingtheabilitytotakeupsulfate werefirstisolatedaschromate/selenate-resistantstrains(Smithetal.,1995b). SeveralofthesemutantstrainswerefoundtohavemutationsinageneSUL1 encodingasulfatetransporter.Thesamestrategyalsoledtotheidentification of two homologous genes, SUL1 and SUL2, encoding sulfate transporters having nearly the same biochemical properties (Cherest et al., 1997). Functional complementation of the yeast sulfate transporter mutant was the strategy used for the identification of plant sulfate transporters. A cDNAlibraryofthelegumeplantspeciesStylosantheshamatawasintroduced intotheyeastmutanttofindclonesthatrestoretheyeastcellgrowthunder low sulfa te su pply (< 0.1 mM )(Smi th et al., 199 5a) . The S.h amataSH ST1, SHST2,andSHST3arethecDNAsidentifiedfromthisscreening.