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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 Firstedition2020 Copyright©2020ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans,electronic ormechanical,includingphotocopying,recording,oranyinformationstorageandretrievalsystem, withoutpermissioninwritingfromthepublisher.Detailsonhowtoseekpermission,further informationaboutthePublisher’spermissionspoliciesandourarrangementswithorganizationssuch astheCopyrightClearanceCenterandtheCopyrightLicensingAgency,canbefoundatourwebsite: www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightbythe Publisher(otherthanasmaybenotedherein). 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ISBN:978-0-12-813180-0 ISSN:0070-2153 ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/books-and-journals Publisher:ZoeKruze EditorialProjectManager:ShellieBryant ProductionProjectManager:DennyMansingh CoverDesigner:GregHarris TypesetbySPiGlobal,India Contributors JamesBriscoe TheFrancisCrickInstitute,London,UnitedKingdom AilinLeticiaBuzzi CentreforCraniofacialandRegenerativeBiology,FacultyofDentistry,Craniofacialand OralSciences,King’sCollegeLondon,London,UnitedKingdom ElisabettaCacace EuropeanMolecularBiologyLaboratory,GenomeBiologyUnit,Heidelberg,Germany Yen-ChungChen DepartmentofBiology,NewYorkUniversity,NewYork,NY,UnitedStates ArielD.Chipman TheDepartmentofEcology,Evolution&Behavior,TheHebrewUniversityofJerusalem, EdmondJ.SafraCampus,GivatRam,Jerusalem,Israel JinS.Cho DepartmentofDevelopmentalandCellBiology,UniversityofCalifornia,Irvine,CA, UnitedStates KenW.Y.Cho DepartmentofDevelopmentalandCellBiology;CenterforComplexBiologicalSystems, UniversityofCalifornia,Irvine,CA,UnitedStates SamuelCollombet EuropeanMolecularBiologyLaboratory,GenomeBiologyUnit,Heidelberg,Germany; ComputationalSystemsBiologyTeam,InstitutdeBiologiedel’E(cid:1)coleNormaleSup(cid:1)erieure (IBENS),CNRS,INSERM,E(cid:1)coleNormaleSup(cid:1)erieure,Universit(cid:1)ePSL,Paris,France M.JoaquinaDela´s TheFrancisCrickInstitute,London,UnitedKingdom ClaudeDesplan DepartmentofBiology,NewYorkUniversity,NewYork,NY,UnitedStates AnnaDiGregorio DepartmentofBasicScienceandCraniofacialBiology,NewYorkUniversityCollegeof Dentistry,NewYork,NY,UnitedStates DouglasH.Erwin DepartmentofPaleobiology,NationalMuseumofNaturalHistory,Washington,DC, UnitedStates RobbKrumlauf StowersInstituteforMedicalResearch,KansasCity,MO;DepartmentofAnatomyandCell Biology,KansasUniversityMedicalCenter,KansasCity,KS,UnitedStates xi xii Contributors EdenMcQueen DepartmentofBiologicalSciences,UniversityofPittsburgh,Pittsburgh,PA,UnitedStates KittD.Paraiso DepartmentofDevelopmentalandCellBiology;CenterforComplexBiologicalSystems, UniversityofCalifornia,Irvine,CA,UnitedStates HugoJ.Parker StowersInstituteforMedicalResearch,KansasCity,MO,UnitedStates IsabelleS.Peter DivisionofBiologyandBiologicalEngineering,CaliforniaInstituteofTechnology, Pasadena,CA,UnitedStates MarkRebeiz DepartmentofBiologicalSciences,UniversityofPittsburgh,Pittsburgh,PA,UnitedStates YutakaSatou DepartmentofZoology,GraduateSchoolofScience,KyotoUniversity,Kyoto,Japan AndreaStreit CentreforCraniofacialandRegenerativeBiology,FacultyofDentistry,Craniofacialand OralSciences,King’sCollegeLondon,London,UnitedKingdom DenisThieffry ComputationalSystemsBiologyTeam,InstitutdeBiologiedel’E(cid:1)coleNormaleSup(cid:1)erieure (IBENS),CNRS,INSERM,E(cid:1)coleNormaleSup(cid:1)erieure,Universit(cid:1)ePSL,Paris,France; CancerScienceInstituteofSingapore,NationalUniversityofSingapore,Singapore, Singapore AlexandreThiery CentreforCraniofacialandRegenerativeBiology,FacultyofDentistry,Craniofacialand OralSciences,King’sCollegeLondon,London,UnitedKingdom JunseokYong DepartmentofDevelopmentalandCellBiology,UniversityofCalifornia,Irvine,CA, UnitedStates RolfZeller DevelopmentalGenetics,DepartmentBiomedicine,UniversityofBasel,Basel,Switzerland Aim(cid:1)eeZuniga DevelopmentalGenetics,DepartmentBiomedicine,UniversityofBasel,Basel,Switzerland Preface Gene regulatory networks (GRNs) offer an unprecedented view on the genomic control of developmental and evolutionary processes.By regulat- ing gene expression, GRNs control the molecular changes in genome activity that drive development and enable evolution. A lot remains to be learned about how GRNs control developmental mechanisms, and this volume provides just a snapshot of a growing field. Many bits and pieces of regulatory circuits have been discovered, or are currently being investi- gated,in different animals andparticularlyalso in plants.In manydevelop- mental contexts, functional analyses of GRNs are starting to illuminate the control systems that generate causality in the developmental process. Thisvolumefocusesinparticularondevelopmentalsystemswheredecades of research have provided sufficient tools and insights to generate a causal understanding of the underlying GRNs and the evolution thereof. The articles in this collection discuss current insights into how GRNs operate in various contexts in development and evolution, and also address some of the challenges that lie ahead and that will be solved in coming years as research in this scientific area advances. The first two chapters of this volume deal with the question of how maternal inputs are interpreted by zygotic GRNs to drive the initial speci- ficationofcellfatesandtocontrolthespatialorganizationofearlyembryos. In Chapter 1, Satou presents a comprehensive account of the GRNs that control the earliest cell fate specification in Ciona embryos. The GRN models compiled in this review explain the specification of cell fates throughouttheembryo,fromtheearliestactivationofthezygoticgenome bymaternaltranscriptionfactorsupto112cellstage.Similarly,inChapter2, Paraiso et al. discuss the initial activation of the zygotic genome by mater- nallylocalizedtranscriptionfactorsinXenopusembryos,withparticularfocus on the endoderm GRN. Later in development, the formation of body parts also depends on the interpretation of localized transcription factors and signaling molecules which define embryonic positions along the major body axes. These regulatory inputs then activate body part-specific GRNs that control the specification and organization of cell fates. In Chapter 3, Zuniga and Zeller review how GRNs control the positioning and specification of the major axes and cell fates in the developing limb of the mouse embryo. xiii xiv Preface These GRNs provide an insightful account for how networks of inter- connectedtranscriptionfactorsandsignalinggradientsestablishthecoordi- nate system that organizes a newly developing body part. The next three chapters deal with the particular challenges of organizing the developing nervous system. Chapter 4 presents a review of the GRNs controlling the specification and coordination of different layers of the visual system in Drosophila, from the specification of progenitor cells to the terminal differ- entiationofdifferenttypesofneurons(ChenandDesplan).Afurtherrapidly growingfieldfocusesonthedevelopmentofvertebratesensoryneuronsand theformationofplacodes.Chapter5presentsacomprehensivereviewofthe GRNs controlling different stages of the specification of placodes, from those defining the progenitors of placodes and neural crest cells to those specifying the diverse types of placodes according to their position along the anterior–posterior axis (Thiery et al.). Organization along the anterior–posterior axis is also crucial in the development of the vertebrate hindbrain. Hox transcription factors play a particularly important role in the control of positional identity of hindbrain rhombomeres, and the regulatory interactions in this GRN have been particularly well explored atthecis-regulatorylevel,asreviewedinChapter6(ParkerandKrumlauf). DevelopmentalGRNscontrollingthespecificationofbodyaxesandcell fates consist of the interactions between many transcriptional regulators, which complicates not only the experimental analysis of these networks, but also the assessment of their system level functions once experimental insights into the players and interactions have been obtained. In order to assess the behavior of these networks and to determine the contribution of individual parts to the overall function of a GRN, more formal analytic approachesbecomenecessary.Chapters7–9addressdifferentapproachesto the computational modeling of network function and to deciphering the function of circuit structure. Chapter 7 presents a detailed account of an approach to Boolean logic modeling of developmental GRNs (Cacace etal.).Ontheotherhand,continuousmodelinghasbeensuccessfullyused to capture the function of a regulatory circuit that forms discrete cell fate domainsinresponsetoasignalinggradient.Thisisparticularlywellresolved inthevertebrateneuraltube,asreviewedbyDela´sandBriscoeinChapter8. Furthermore, a comparison of the topology of various GRNs indicates that network structure and regulatory logic have an important function in the system level control of developmental processes, as discussed in Chapter 9 (Peter). Preface xv The evolution of the animal body plan is a challenging topic to address experimentally as well as conceptually. The growing understanding of developmental GRNs provides an important opportunity in this field. By viewing animal evolution as the outcome of change of developmental processes,andthereforeofchangeindevelopmentalGRNs,severalevolu- tionarymechanismshavebeendiscoveredthatexplainevolutionarychange as well as conservation. The last four chapters in this volume address this topic. From an experimental perspective, Chapter 10 summarizes recent insights into the GRNs controlling segmentation in different arthropods and shows how these findings can illuminate the possible evolutionary history of this network (Chipman). Similarly, Chapter 11 discusses the evolution of the notochord GRN, starting from the perspective of the Ciona GRN and its relevance to understanding the evolution of the notochord GRN in vertebrates (Di Gregorio). And finally, the last two chapters of this volume address the mechanisms of evolutionary change in GRNs.Chapter12discussesthepossibleconsequencesoftheevolutionary co-optionoftranscriptionfactorsornetworksubcircuitstonoveldevelop- mental contexts (McQueen and Rebeiz). Chapter 13 provides a more general overview of evolutionary changes that enabled adaptations as well asmacroevolutionarychangeofthebodyplanandconsidershowevolution- ary modifications of the regulatory genome have contributed to the generation of morphological novelty (Erwin). Just about 50 years ago, in 1969, Roy Britten and Eric Davidson envisioned a first model for how gene regulation occurs during animal development. Although it would take several decades before this problem became accessible to experimental analysis, this model was nevertheless fundamental for the discovery of GRNs that control genome activity in development. This volume is a celebration of the intellectual, technical, andexperimentalachievementsthathavecontributedtothecurrentinsights into the control systems in so many developmental and evolutionary processes. ISABELLE S. PETER Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, United States CHAPTER ONE A gene regulatory network for Ciona cell fate specification in embryos Yutaka Satou* DepartmentofZoology,GraduateSchoolofScience,KyotoUniversity,Kyoto,Japan *Correspondingauthor:e-mailaddress:[email protected] Contents 1. Introduction 2 2. Basicpropertiesforthegeneregulatorynetworkinearlyascidianembryos 4 2.1 Regulatorygenes 4 2.2 Initialconditionsforthegeneregulatorynetwork 5 2.3 Outputsofthegeneregulatorynetwork 5 2.4 Potentiallyuniquepropertiesofthegeneregulatorynetworkinearly ascidianembryos 7 3. Thegeneregulatorynetworkaccountsforchangesofgeneexpressioninspace andtime 10 3.1 Theinitialsetupinthe16-cellembryobymaternalfactors 10 3.2 Specificgeneexpressioninthe32-cellembryo 12 3.3 Specificgeneexpressionatthe64-cellstageandthereafter 16 4. Perspectives 25 References 26 Abstract Ascidianembryosareusedasamodelsystemindevelopmentalbiologyduetotheir uniqueproperties,includingtheirinvariantcelldivisionpatterns,beingcomprisedof asmallnumberofcellsandtissues,thefeasibilityoftheirexperimentalmanipulation, andtheirsimpleandcompactgenome.Thesepropertieshaveprovidedanopportunity for examining the gene regulatory network at the single cell resolution and at a genome-wide scale. This article summarizes when and where each regulatory gene isexpressed in early ascidian embryos, andthe extent to which thegene regulatory networkexplainseachgeneexpression. CurrentTopicsinDevelopmentalBiology,Volume139 #2020ElsevierInc. 1 ISSN0070-2153 Allrightsreserved. https://doi.org/10.1016/bs.ctdb.2020.01.001 2 YutakaSatou 1. Introduction Ascidians are invertebrate chordates that have been used in research for over 100 years, since the studies in 1905 by Conklin (1905a, 1905b, 1905c).Celldivisionpatternsinascidianembryosareinvariantamongindi- viduals,andcellsareeasilyidentifiableunderabinocularstereomicroscope. Takingadvantageofthesefeatures,eachcellisuniquelynamed,andcelllin- eages have been traced (Conklin, 1905c; Nishida, 1987; Nishida & Satoh, 1983, 1985). These experiments have revealed that most cells obtain one uniquedevelopmentalfatebythe112-cellstage(Fig.1A).Thatis,individual cells in the 112-cell embryos are precursors for cells that appear in neurula tolarvalstages(Fig.1BandC).Inotherwords,celltypesthatarefoundin A vegetal hemisphere animal hemisphere posterior neural plate (PNP) anterior neural plate (ANP) (Zic-r.b, Foxb) (Zic-r.b, Dmrt.a) notochord (T) anterior neural plate border (ANB) (Foxc, Dmrt.a) lateral neural plate and its border (LNPB) (Nodal, Zic-r.b) B8.15 mesenchyme (Twist-r) muscle (Mrf) muscle/heart precursor (Mrf/Mesp) epidermis (Tfap2-r.b, Dlx.b) endoderm germ cells (Lhx3/4, Nkx2-1/4) (Pem-1) B ANBANP PNP C central nervous systemepidermis nterior LNPB osterior notochord a p mesenchyme muscle palp endoderm Fig.1 DevelopmentofCionaembryos.(A)Illustrationsforthevegetal(left)andanimal views(right)ofthe112-cellembryo(approximately4.5hafterfertilizationat18°C).Cells with different developmental fates are marked with different patterns and colors. Representative genes expressed in individual lineages are shown in parentheses. (B)Illustrationoftheinitialneurula(approximately6hafterfertilizationat18°C)show- ingtheneuralplateanditsborderregion.(C)Illustrationoflarvawithsimplearchitec- ture.Thetadpolelarvahatchesin18hafterfertilizationat18°C.