CURRENT TOPICS IN DEVELOPMENTAL BIOLOGY “Ameeting-groundforcriticalreviewanddiscussionofdevelopmentalprocesses” A.A.MosconaandAlbertoMonroy(Volume1,1966) SERIES EDITOR Paul M. Wassarman DepartmentofCell,DevelopmentalandRegenerativeBiology IcahnSchoolofMedicineatMountSinai NewYork,NY,USA CURRENT ADVISORY BOARD Blanche Capel Susan Mango Wolfgang Driever Philippe Soriano Denis Duboule Cliff Tabin Anne Ephrussi MagdalenaZernicka-Goetz FOUNDING EDITORS A.A. Moscona and Alberto Monroy FOUNDING ADVISORY BOARD Vincent G. Allfrey Dame Honor B.Fell Jean Brachet John C. Kendrew Seymour S. Cohen S.Spiegelman Bernard D.Davis Hewson W.Swift James D. Ebert E.N.Willmer Mac V. Edds, Jr. Etienne Wolff AcademicPressisanimprintofElsevier 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom 125LondonWall,London,EC2Y5AS,UnitedKingdom Firstedition2019 Copyright©2019ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices, ormedicaltreatmentmaybecomenecessary. Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors, assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods, products,instructions,orideascontainedinthematerialherein. ISBN:978-0-12-809804-2 ISSN:0070-2153 ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/books-and-journals Publisher:ZoeKruze AcquisitionEditor:FionaPattison EditorialProjectManager:ShellieBryant ProductionProjectManager:DennyMansingh CoverDesigner:GregHarris TypesetbySPiGlobal,India Contributors AlmaArmenta-Medina LaboratorioNacionaldeGeno´micaparalaBiodiversidad(Langebio),UnidaddeGeno´mica Avanzada,CentrodeInvestigacio´nyEstudiosAvanzadosdelInstitutoPolit(cid:1)ecnicoNacional (CINVESTAV-IPN),Irapuato,Guanajuato,M(cid:1)exico C(cid:1)eliaBaroux DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland JohnL.Bowman SchoolofBiologicalSciences,MonashUniversity,Melbourne,VIC,Australia LiamN.Briginshaw SchoolofBiologicalSciences,MonashUniversity,Melbourne,VIC,Australia JohnW.Chandler DepartmentofBiology,Biocenter,UniversityofCologne,Cologne,Germany MartaCubr´ıa-Rad´ıo DepartmentofPlantBiotechnologyandBioinformatics,GhentUniversity;VIBCenterfor PlantSystemsBiology,Ghent,Belgium MainakDasGupta MaxPlanckInstituteforPlantBreedingResearch,Cologne,Germany ThomasDresselhaus CellBiologyandPlantBiochemistry,UniversityofRegensburg,Regensburg,Germany StevieN.Florent SchoolofBiologicalSciences,MonashUniversity,Melbourne,VIC,Australia HirooFukuda DepartmentofBiologicalSciences,GraduateSchoolofScience,TheUniversityofTokyo, Tokyo,Japan CharlesS.Gasser DepartmentofMolecularandCellularBiology,UniversityofCalifornia,Davis,Davis,CA, UnitedStates C.StewartGillmor LaboratorioNacionaldeGeno´micaparalaBiodiversidad(Langebio),UnidaddeGeno´mica Avanzada,CentrodeInvestigacio´nyEstudiosAvanzadosdelInstitutoPolit(cid:1)ecnicoNacional (CINVESTAV-IPN),Irapuato,Guanajuato,M(cid:1)exico RitaGroß-Hardt CentreforBiomolecularInteractions,UniversityofBremen,Bremen,Germany UeliGrossniklaus DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland xiii xiv Contributors DieterHackenberg DepartmentofGeneticsandGenomeBiology,UniversityofLeicester,Leicester, UnitedKingdom AlexanderKirbis DepartmentofSystematicandEvolutionaryBotany&Zurich-BaselPlantScienceCenter, UniversityofZurich,Zurich,Switzerland ElenaM.Kramer HarvardUniversity,Cambridge,MA,UnitedStates GloriaLeo´n-Mart´ınez GroupofReproductiveDevelopmentandApomixis,UGALaboratorioNacionalde Geno´micaparalaBiodiversidad(Langebio),CinvestavIrapuato,Irapuato,Mexico JuneB.Nasrallah SectionofPlantBiology,SchoolofIntegrativePlantScience,CornellUniversity,Ithaca, NY,UnitedStates LachezarA.Nikolov MaxPlanckInstituteforPlantBreedingResearch,Cologne,Germany MoritzK.Nowack DepartmentofPlantBiotechnologyandBioinformatics,GhentUniversity;VIBCenterfor PlantSystemsBiology,Ghent,Belgium KyokoOhashi-Ito DepartmentofBiologicalSciences,GraduateSchoolofScience,TheUniversityofTokyo, Tokyo,Japan LarsØstergaard DepartmentofCropGenetics,JohnInnesCentre,Norwich,UnitedKingdom JoakimPalovaara CentreforBiomolecularInteractions,UniversityofBremen,Bremen,Germany JohnB.Reese DepartmentofEcologyandEvolutionaryBiology,UniversityofTennessee,Knoxville,TN, UnitedStates AdamRunions MaxPlanckInstituteforPlantBreedingResearch,Cologne,Germany IsilErbasolSerbes CentreforBiomolecularInteractions,UniversityofBremen,Bremen,Germany VinayShekhar DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland BihaiShi LaboratoireReproductionetDeveloppementdesPlantes,UnivLyon,ENSdeLyon,UCB Lyon1,CNRS,INRA,Lyon,France Contributors xv SaraSimonini DepartmentofCropGenetics,JohnInnesCentre,Norwich,UnitedKingdom DebraJ.Skinner DepartmentofMolecularandCellularBiology,UniversityofCalifornia,Davis,Davis,CA, UnitedStates DorotheeSto€ckle DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland P(cid:1)eterSzo€v(cid:1)enyi DepartmentofSystematicandEvolutionaryBotany&Zurich-BaselPlantScienceCenter, UniversityofZurich,Zurich,Switzerland MarthaThellmann DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland BennettThomson SmurfitInstituteofGenetics,TrinityCollegeDublin,Dublin,Ireland MiltosTsiantis MaxPlanckInstituteforPlantBreedingResearch,Cologne,Germany DavidTwell DepartmentofGeneticsandGenomeBiology,UniversityofLeicester,Leicester, UnitedKingdom KarinavanderLinde DepartmentofCellBiologyandPlantBiochemistry,UniversityofRegensburg, Regensburg,Germany JoopE.M.Vermeer DepartmentofPlantandMicrobialBiology&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland TevaVernoux LaboratoireReproductionetDeveloppementdesPlantes,UnivLyon,ENSdeLyon,UCB Lyon1,CNRS,INRA,Lyon,France Jean-PhilippeVielle-Calzada GroupofReproductiveDevelopmentandApomixis,UGALaboratorioNacionalde Geno´micaparalaBiodiversidad(Langebio),CinvestavIrapuato,Irapuato,Mexico VirginiaWalbot DepartmentofBiology,StanfordUniversity,Stanford,CA,UnitedStates ManuelWaller DepartmentofSystematicandEvolutionaryBotany&Zurich-BaselPlantScienceCenter, UniversityofZurich,Zurich,Switzerland FrankWellmer SmurfitInstituteofGenetics,TrinityCollegeDublin,Dublin,Ireland xvi Contributors WolfgangWerr DepartmentofBiology,Biocenter,UniversityofCologne,Cologne,Germany JosephH.Williams DepartmentofEcologyandEvolutionaryBiology,UniversityofTennessee,Knoxville,TN, UnitedStates Liang-ziZhou CellBiologyandPlantBiochemistry,UniversityofRegensburg,Regensburg,Germany Preface Plantsarethebasisoflifeonearthasweknowitandhavenotonlyshaped,to alargeextent,diverseecosystemsbutalsoprovidefood,feed,fibers,andfuel for human subsistence. Understanding how plants evolved and develop to fulfill their manifold functions is thus of great fundamental and applied interest. It will soon be 10 years since the last volume of Current Topics in Developmental Biology focused on plant development. Since then, biology has seen a revolution in methods for the investigation of genes, transcripts, andproteins,allowingawidevarietyof“omics”approaches.Also,thetools to investigate gene function using forward-genetic, reverse-genetic, and alternative methods, such as artificial microRNAs and RNA interference, haveprovideddeepinsightsintothemolecularprocessesthatregulateplant development.Thearsenaloftheplantbiologisthasrecentlybeenextended bytheCRISPR/Cas9system,whichallowsfunctionalstudiesalsoinnon- model systems, providing new insights into developmental diversity and plasticity.Clearly,focusingeffortsonamodelsystem,inthiscaseArabidopsis thaliana,hasgreatlyacceleratedprogressinunderstandingplantfunction.On theotherhand,atunnelvisionfocusingonasinglespeciesisboundtomiss important aspects of development that are not found in this model system. Certainly,plantbiologyhasprofitedalotfromthepowerfulgeneticsofZea mays (maize), which started well over a hundred years ago, and the recent focusonOryzasativa(rice)asoneofthemostimportantcrop plants.Over the last years, the range of plant species used in fundamental research has greatly expanded, providing insights into diverse developmental processes. Unraveling the molecular control of plant development has also providedthematerialtolookattheevolutionofgeneregulatorynetworks, investigatinghowpreexistingmechanismswereco-optedfornewdevelop- mental programs or how novelties arose during land plant evolution. Such evo-devo studies have provided great insights into the evolution of the enormous diversity of plants that exists today. It is more than timely then toprovideabroadoverviewofplantdevelopmentandevolution,asitisonly possibleinamultichapterbookbringingtogetherexpertsindiversefieldto sharetheirviewsonspecificplantdevelopmentalprocessesandtheirevolu- tion.Thechaptersprovideawidediversityofperspectivesonbothvegeta- tive and reproductive development, summarizing the deep functional and xvii xviii Preface mechanistic insights that have been gained in many fields of development. Thechaptersfocusingonevolutionaryaspectsprovideanexcellentviewon thedirectionstheevo-devofieldwilltakeinthefuturebybeingabletodo functional studies in nonmodel systems that promise to provide invaluable insights into the evolution of plant development. Iwasdelightedthatsomanyofmycolleaguesenthusiasticallyacceptedto contributetothisvolumeofCurrentTopicsinDevelopmentalBiologyandIam thankfulfortheirdetailedreviewsandinsightfuldiscussionsonawiderange oftopicsinplantdevelopmentandevolution.Nodoubtthenextdecadewill seeenormousprogressandfurtherdeepenourunderstandingofplantfunc- tion. Nevertheless, I am convinced that the readers will find this volume interesting and timely and hope they will enjoy reading it. UELI GROSSNIKLAUS Department of Plant and Microbial Biology & Zurich-Basel Plant Science Center, University of Zurich, Zurich, Switzerland ARTICLE IN PRESS Evolution of the plant body plan Pe(cid:1)ter Szo€ve(cid:1)nyi*, Manuel Waller, Alexander Kirbis DepartmentofSystematicandEvolutionaryBotany&Zurich-BaselPlantScienceCenter,University ofZurich,Zurich,Switzerland *Correspondingauthor:e-mailaddress:[email protected] Contents 1. Thesignificanceoflandplants 2 2. Understandingevolutionoftheplantbodyplan 2 3. Phylogeneticrelationshipsoflandplantsandevolutionofthelandplant bodyplan 3 4. Developmentalpatternspredatingtheoriginoflandplants 5 5. Developmentalinnovationsoflandplants 7 5.1 Alternationofhaploid(gametophyte)anddiploid(sporophyte) generations 7 5.2 Evolutionofthree-dimensionalgrowthinthehaploidanddiploidphases 10 5.3 Originofspores,sporangia,andsporopollenininlandplants 12 5.4 Originofunbranchedsporophyteforms 12 5.5 Evolutionofbifurcatingaxes 14 5.6 Evolutionofindeterminacy 15 5.7 Evolutionofmeristems 16 5.8 Originofleaves 17 5.9 Evolutionofrootingsystems 20 5.10 Roots 22 6. Conclusionsandperspectives 24 Acknowledgments 25 References 25 Abstract Landplantsevolvedabout470millionyearsagoorevenearlier,inabiologicalcrust- dominatedterrestrialflora.Theoriginoflandplantswasprobablyoneofthemostsig- nificanteventsinEarth’shistory,whichultimatelycontributedtothegreeningofthe terrestrial environment and opened up the way for the diversification of both plant andnon-plantlineages.Fossilandphylogeneticevidencesuggestthatlandplantshave evolvedfromfresh-watercharophyceanalgae,whichwerephysiologically,genetically, anddevelopmentallypotentiatedtomakethetransitiontoland.Sincealllandplants have biphasic life cycles, in contrast to the haplontic life cycle of Charophytes, the evolutionoflandplantswaslinkedtotheoriginofamulticellularsporophyticphase. Land plants have evolved complex body plans in a way that overall complexity CurrentTopicsinDevelopmentalBiology #2018ElsevierInc. 1 ISSN0070-2153 Allrightsreserved. https://doi.org/10.1016/bs.ctdb.2018.11.005