An update on carotenoid biosynthesis in algae

Planta(2009)229:723–729DOI10.1007/s00425-008-0866-2123SHORTCOMMUNICATIONAnupdateoncarotenoidbiosynthesisinalgae:phylogeneticevidencefortheexistenceoftwoclassesofphytoenesynthaseDucTran·JamesHaven·Wei-GangQiu·JuergenE.W.PolleReceived:2October2008/Accepted:17November2008/Publishedonline:9December2008©Springer-Verlag2008AbstractCarotenoidsplaycrucialrolesinstructureandfunctionofthephotosyntheticapparatusofbacteria,algae,andhigherplants.Theentry-stepreactiontocarotenoidbio-synthesisiscatalyzedbythephytoenesynthase(PSY),whichisstructurallyandfunctionallyrelatedinallorgan-isms.AcomparativegenomicanalysisregardingthePSYrevealedthatthegreenalgaeOstreococcusandMicro-monaspossesstwoorthologouscopiesofthePSYgenes,indicatinganancientgeneduplicationeventthatproducedtwoclassesofPSYinalgae.However,someothergreenalgae(Chlamydomonasreinhardtii,Chlorellavulgaris,andVolvoxcarteri),redalgae(Cyanidioschyzonmerolae),dia-toms(ThalassiosirapseudonanaandPhaeodactylumtri-cornutum),andhigherplantsretainedonlyoneclassofthePSYgenewhereastheothergenecopywaslostinthesespecies.Further,similartothesituationinhigherplantsrecentgeneduplicationsofPSYhaveoccurredforexampleinthegreenalgaDunaliellasalina/bardawil.AsmembersofthePSYgenefamiliesinsomehigherplantsarediVeren-tiallyregulatedduringdevelopmentorstress,thediscoveryoftwoclassesofPSYgenefamiliesinsomealgaesuggeststhatcarotenoidbiosynthesisinthesealgaeisdiVerentiallyregulatedinresponsetodevelopmentandenvironmentalstressaswell.KeywordsAlgae·Carotenoidbiosynthesis·PhytoenesynthaseAbbreviationsPSYPhytoenesynthaseIntroductionCarotenoidsareisoprenoidswhichderivedfromtheprecur-sormoleculeisopentenylpyrophosphateanditsisomerdimethylallyldiphosphate.Allphotosyntheticorganismsincludinghigherplantsandalgaesynthesizecarotenoids(ArmstrongandHearst1996;CunninghamandGantt1998;DellaPennaandPogson2006;FraserandBramley2004;Goodwin1980;Hirschbergetal.1997;Lichtenthaler1999)whicharestructurallyconstitutedinthethylakoidmem-braneandfunctionasaccessorymoleculesforlightharvest-ingandforpreventionfromphoto-damageandasantioxidantsunderstressconditions(Goodwin1980;Hirschbergetal.1997;McCarthyetal.2004;DellaPennaandPogson2006;Lichtenthaler2007).Thephytoenesynthase(PSY)isconsideredastheenzymeperformingtherate-limitingentryreactionintothecarotenoidbiosynthesispathwayinphotosyntheticorgan-isms(Chenetal.2007;Lindgrenetal.2003;Salvinietal.2005;Yanetal.2005;Lietal.2008b).MultipleparalogousPSYgeneswerediscoveredinhigherplantssuchascorn(Lietal.2008a,b)andtomato(BartleyandScolnik1993)inwhichchromoplastsofspecializedtissuecellsover-accu-mulatecarotenoids.WhenparalogousgenesexistinhigherplantstheyareoftendiVerentiallyup-regulateddependingD.Tran·J.E.W.Polle(&)DepartmentofBiology,BrooklynCollegeoftheCityUniversityofNewYork,2900BedfordAvenue200NE,Brooklyn,NY11210,USAe-mail:[e-mail],StJohn’sUniversity,8000UtopiaParkwayJamaica,NewYork,NY11439,USAJ.Haven·W.-G.QiuDepartmentofBiologicalSciences,HunterCollegeoftheCityUniversityofNewYork,695ParkAvenue,NewYork,NY10065,USA724Planta(2009)229:723–729123onenvironmentalconditionsordevelopmentalstagesofvari-oustissues(BartleyandScolnik1993;Buckneretal.1996;Lietal.2008b).Inthepastbiosynthesisofcarotenoidsofbacteriaandhigherplantshasbeenstudiedextensively,whereasresearchoncarotenoidbiosynthesisinalgaeisstillinitsinfancy.Forunicellulargreenalgae,PSYwasprevi-ouslyinvestigatedforexampleinChlamydomonasreinhardtii(BohneandLinden2002;McCarthyetal.2004;Lohretal.2005)andHaematococcuspluvialis/lacustris(SteinbrennerandLinden2001).ThegenomeofC.rein-hardtiicontainsonlyonefunctionalpsygene(McCarthyetal.2004;Lohretal.2005).ForHaematococcusthenum-berofpsycopiespergenomeisunknown,butpsywasshowntobeup-regulatedunderstressconditionsofhighlightandlownutrientavailability(SteinbrennerandLinden2001,2003).Further,psygeneswerealsoclonedfromdiVer-entspeciesoftheunicellulargreenalgaDunaliella(Yanetal.2005),butsofaronlyonegenewasreportedforeachspecies.Recently,thegenomesequencesforanumberofdiVer-entmicroalgaebecameavailablefromtheDOEJointGenomeInstitute(http://www.jgi.doe.gov).Anexamina-tionofthesealgaegenomeswithrepresentativesfromverydiVerentgroupssuchasgreenalgae,redalgae,diatoms,andhaptophyteswasperformedtoidentifytheirpsygenes.Theresultspresentedheredemonstratethatsomealgaecontainonlyasinglegenecodingforpsywhereasotheralgaecon-taineithermultipleparalogousororthologouscopiesofthepsy.FromthediscoveryofsmallpsygenefamiliesinalgaeitcanbeexpectedthatanalogoustothediversityofpsygenesandtheirdiVerentialexpressioninhigherplants(Lietal.2008a,b)algaealsodiVerentiallyregulateexpressionoftheirparalogouspsygenecopies.Similarly,itmaybehypothesizedthatorthologouspsygenecopiesidentiWedinsomealgaecouldalsobediVerentiallyregulated.MaterialsandmethodsPhytoenesynthasecDNAandproteinsequencesofAureo-coccusanophageVerens,Chlamydomonasreinhardtii,Chlorellasp.NC64A,Volvoxcarteri,Micromonaspusilla,Micromonassp.RCC299,Ostreococcuslucimarinus,Ost-reococcustauri,OstreococcusRCC809,Emilianiahuxleyi,Thalass