Maternal Effect Genes in Development

431 Pages·2020·16.794 MB·English

by  Florence Marlow

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).
Notices
Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchandexperience
broadenourunderstanding,changesinresearchmethods,professionalpractices,ormedical
treatmentmaybecomenecessary.
Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgeinevaluating
andusinganyinformation,methods,compounds,orexperimentsdescribedherein.Inusingsuch
informationormethodstheyshouldbemindfuloftheirownsafetyandthesafetyofothers,including
partiesforwhomtheyhaveaprofessionalresponsibility.
Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors,assume
anyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterofproductsliability,
negligenceorotherwise,orfromanyuseoroperationofanymethods,products,instructions,orideas
containedinthematerialherein.
ISBN:978-0-12-815220-1
ISSN:0070-2153
ForinformationonallAcademicPresspublications
visitourwebsiteathttps://www.elsevier.com/books-and-journals
Publisher:ZoeKruze
EditorialProjectManager:ShellieBryant
ProductionProjectManager:DennyMansingh
CoverDesigner:GregHarris
TypesetbySPiGlobal,India
Contributors
ElliottW.Abrams
DepartmentofBiology,PurchaseCollege,StateUniversityofNewYork,Harrison,NY,
UnitedStates
BenE.Black
DepartmentofBiochemistryandBiophysics,PerelmanSchoolofMedicine,Universityof
Pennsylvania,Philadelphia,PA,UnitedStates
PatrickBlatt
DepartmentofBiologicalSciences/RNAInstitute;UniversityatAlbanySUNY,Albany,
NY,UnitedStates
ShaneM.Breznak
DepartmentofBiologicalSciences/RNAInstitute;UniversityatAlbanySUNY,Albany,
NY,UnitedStates
SarahE.Cabral
DepartmentofMolecularBiology,CellBiology,andBiochemistry,BrownUniversity,
Providence,RI,UnitedStates
ArunikaDas
DepartmentofBiology;DepartmentofBiochemistryandBiophysics,PerelmanSchoolof
Medicine,UniversityofPennsylvania,Philadelphia,PA,UnitedStates
JurrienDean
LaboratoryofCellularandDevelopmentalBiology,NIDDK,NationalInstitutesofHealth,
Bethesda,MD,UnitedStates
MatthewM.S.Evans
DepartmentofPlantBiology,CarnegieInstitutionforScience,Stanford,CA,UnitedStates
RicardoFuentes
DepartamentodeBiolog´ıaCelular,FacultaddeCienciasBiolo´gicas,Universidadde
Concepcio´n,Concepcio´n,Chile
KristaR.Gert
ResearchInstituteofMolecularPathology(IMP),ViennaBioCenter(VBC),Vienna,Austria
TheresaGross-Thebing
InstituteofAnatomyandVascularBiology,UniversityofMu€nster,Mu€nster,Germany
ManamiKobayashi
DepartmentofCellandDevelopmentalBiology,UniversityofPennsylvania,Perelman
SchoolofMedicine,Philadelphia,PA,UnitedStates
MichaelA.Lampson
DepartmentofBiology,UniversityofPennsylvania,Philadelphia,PA,UnitedStates
YvetteLangdon
MillsapsCollege,Jackson,MS,UnitedStates
xi
xii Contributors
ThierryLepage
InstitutdeBiologieValrose,Universit(cid:2)eCo^ted’Azur,Nice,France
ElliotT.Martin
DepartmentofBiologicalSciences/RNAInstitute;UniversityatAlbanySUNY,Albany,
NY,UnitedStates
JulieA.Merkle
DepartmentofBiology,UniversityofEvansville,Evansville,IN,UnitedStates
MariaDoloresMolina
InstitutdeBiologieValrose,Universit(cid:2)eCo^ted’Azur,Nice,France
CaraE.Moravec
LaboratoryofGenetics,UniversityofWisconsin—Madison,Madison,WI,UnitedStates
KimberlyL.Mowry
DepartmentofMolecularBiology,CellBiology,andBiochemistry,BrownUniversity,
Providence,RI,UnitedStates
MaryC.Mullins
DepartmentofCellandDevelopmentalBiology,UniversityofPennsylvania,Perelman
SchoolofMedicine,Philadelphia,PA,UnitedStates
AndreaPauli
ResearchInstituteofMolecularPathology(IMP),ViennaBioCenter(VBC),Vienna,Austria
FranciscoPelegri
LaboratoryofGenetics,UniversityofWisconsin—Madison,Madison,WI,UnitedStates
JoseL.Pelliccia
DepartmentofCellandDevelopmentalBiology,UniversityofPennsylvania,Perelman
SchoolofMedicine,Philadelphia,PA,UnitedStates
AllisonR.Phillips
BiologyDepartment,WisconsinLutheranCollege,Milwaukee,WI,UnitedStates
PrashanthRangan
DepartmentofBiologicalSciences/RNAInstitute;UniversityatAlbanySUNY,Albany,
NY,UnitedStates
ErezRaz
InstituteofCellBiology,UniversityofMu€nster,Mu€nster,Germany
TrudiSchu€pbach
DepartmentofMolecularBiology,PrincetonUniversity,Princeton,NJ,UnitedStates
LiliannaSolnica-Krezel
DepartmentofDevelopmentalBiologyandCenterofRegenerativeMedicine,Washington
UniversitySchoolofMedicine,St.Louis,MO,UnitedStates
BenjaminTajer
DepartmentofCellandDevelopmentalBiology,UniversityofPennsylvania,Perelman
SchoolofMedicine,Philadelphia,PA,UnitedStates
Contributors xiii
NadineL.Vastenhouw
MaxPlanckInstituteofMolecularCellBiologyandGenetics,Dresden,Germany
JuliaWittes
DepartmentofBiologicalSciences,ColumbiaUniversity,NewYork,NY,UnitedStates
DiWu
LaboratoryofCellularandDevelopmentalBiology,NIDDK,NationalInstitutesofHealth,
Bethesda,MD,UnitedStates
EdlynWu
MaxPlanckInstituteofMolecularCellBiologyandGenetics,Dresden,Germany
Preface
“Whenyoustartwithaportraitandsearchforapureform,aclearvolume,
throughsuccessiveeliminations,youarriveinevitably attheegg.Likewise,
startingwiththeeggandfollowingthesameprocessinreverse,onefinishes
with the portrait” (Pablo Picasso). Like Picasso’s portrait, if one starts with
an embryo and tries to understand its form you arrive at production of
the maternal gamete, the oocyte or egg. This meiotic cell forms from the
differentiating divisions of mitotically dividing germline stem cells in the
ovaryoffemales.WhenIbeganassemblingthisvolumeonmaternalcontrol
of development, I envisioned that the chapters in the first section would
begin with that “pure form” reviewing what is known of the cellular and
molecular mechanisms underlying formation of the egg, including the
mitotic to meiotic switch and oogenesis,RNA regulation, and inheritance
of maternal factors in model organisms, including plants. From there, the
second section would focus on fertilization of the egg, specification of the
germline, clearance of maternal factors, and activation of zygotic genome.
Finally, the third part of the volume would feature chapters on the cellular
and molecular mechanisms underlying embryonic axis determination,
including maternal factors that induce and pattern the germ layers across
model systems. Although the details are somewhat varied the molecular
playersareremarkablyconserved.Thevolumeconcludeswithprocessesthat
arecoordinatedbybothmaternalandzygoticprograms.Withcontributions
from many experts, 13 chapters of this volume of Current Topics in
Developmental Biology collectively paint a clear portrait of the current state
of the field.
Our understanding of how the immortal germline transits through
distinct cell cycle and differentiation programs has flourished considerably
over the years from genetic and biochemical studies in model systems.
Based on the work of many labs utilizing various model systems, it is
apparent that much of this regulation is accomplished in large part at the
posttranscriptional level, via regulation of translation, localization, and
stabilityofRNA.Itiswellappreciatedthatvaststoresofmaternalproducts,
including RNAs and proteins are amassed in the oocyte and that these
maternal stores are transmitted to the progeny to support the earliest
developmental events. Yet, we still do not fully understand how this
maternal dowry is regulated, which machinery and factors ensure that
xv
xvi Preface
thereservesarepreserveduntiltheyareneededandareonlydiscardedwhen
theirfunctionhasbeenfulfilled.InChapter1,PatrickBlatt,ElliotT.Martin,
Shane M. Breznak, and Prashanth Rangan review recent advances in our
understanding of the contributions of evolutionarily conserved factors and
pathways to posttranscriptional control of RNA production, turnover,
andexpressionaffordedbyhigh-throughputsequencingandgeneticstudies
withafocusonthestemcelltooocytetransitioninDrosophilamelanogaster.
The contribution of factors that are transmitted independent of the
genome one inherits, or epigenetic regulation has become an increasingly
recognized and important feature of the mechanisms underlying develop-
mental and homeostatic processes. In the context of maternal-effects,
extragenomic or DNA sequence independent influencers of regulation
havebeenconsideredtoincludeallfactorswithtransgenerationalinfluences
on the immediate progeny or grandchildren, including maternal diet,
metabolism, or health, as well as the centromere-based mechanisms that
ensure faithful separation of the chromosomes during meiotic divisions.
InChapter2,ArunikaDas,BenE.Black,andMichaelA.Lampsonexplore
new developments in our understanding of the mechanisms governing
inheritanceofthecentromeresinthematernalgermlineandposeunsolved
and emerging questions about meiotic drive, centromere architecture, and
propagation of centromeres from diverse species.
Of course, no successful endeavor is realized without tremendous
support, and production of a developmentally competent oocyte or egg is
noexception.Throughoutthecourseofitsdevelopment,theoocyteisfully
supported by the somatic cells that surround, signal to, and nourish the
developing gamete. These support cells that comprise the somatic gonad
are commonly known to reproductive biologists as follicle cells because
they, together with the germline cell, form the developing follicle.
Follicle cells come in several types ranging from a couple of distinct cell
typesfoundininvertebratesystemstotheincreasinglycomplexmultilayered
and multicell types found in maturing vertebrate and mammalian ovarian
follicles. Regardless of the degree of relative complexity, oocyte develop-
ment and egg production absolutely depend on the follicle cells of the
somatic gonad, as well as the extragonadal signals that these cells receive
and transmit from other organ systems to maintain reproductive health.
In Chapter 3, Julie A. Merkle, Julia Wittes, and Trudi Schu€pbach review
the genetic mechanisms that establish distinct follicle cell types, and the
contributions of these unique somatic fates to signaling and patterning of
the Drosophila egg.
Preface xvii
In many species, the cytoplasm of the oocyte is not homogeneous;
proteins, RNAs, and organelles have been observed to be asymmetrically
distributedatspecifichallmarkstagesinnearlyeveryspeciesexaminedthus
far.Notably,althoughtheseorganellesandmoleculesaresequesteredwithin
cells, they are not bound by membrane enclosed compartments. Instead,
theyresideinbiochemicallyuniqueenvironmentsthatarethoughttoform
through a process of phase separation. Importantly, these subcellular
environments are not unique quirks of oocytes, but rather represent a
broader mechanism to control expression of the cellular transcriptome,
potentiallyallowingformorepreciseandrapidresponsestochangingcellu-
larenvironments.Chapter4ofthisvolumebySarahE.CabralandKimberly
L. Mowry provides insight into this regulatory mechanism gleaned from
studies of RNA localization and phase separation in vertebrate oocytes.
Withtheexceptionofparthenogenesisthatoccursinsomeinvertebrates
and plants, even a perfectly formedegg willnot develop further unlessit is
fertilized. Gametes of sexually reproducing species are haploid, each with
only half the number of chromosomes necessary to make an individual.
Infemalegametesofsomespecies,thefinalmeioticdivisionoccursintan-
demwitheggactivationorfertilization.Inallsexuallyreproducinganimals,
mechanismsareinplacetoensurethataneggisfertilizedbyonlyonesperm,
thus restoring ploidy and generating an individual with roughly half the
chromosomes of maternal origin and the other of paternal origin. These
mechanismsinvolveprocessesthatareintrinsictotheeggaswellasprocesses
governed by the zona or eggshell structure that is produced in partnership
between the germline and somatic follicle cells, as well as interactions
between the egg and sperm. In Chapter 5, Krista R. Gert and Andrea
Pauli examine the mechanisms regulating species-specific interactions
between gametes for animals with external fertilization as well as the
moleculesandfactorsmediatingactivationoftheeggtopromotesuccessful
fertilization and prevent polyspermy.
The newly fertilized egg has the potential to make every cell type that
comprises the individual, including all the germ layers and cell types that
makeuptheorgansystemsofthespecies.Givenitsvitalroleinperpetuation
of the species, it is no surprise that specification of the germline occurs
during early development in many organisms. In some animals, but not
all,thegermlineisspecifiedbyandfullydependentonamaternallyinherited
program. In others a maternal program is present but can be replaced by
an inductive zygotic mechanism if the maternal program fails. Finally,
some species, including mammals lack a maternal program for germline
xviii Preface
specificationandinsteadrelyonaninductivezygoticpathway.Chapter6by
CaraE.MoravecandFranciscoPelegrifocusesonthecellularandmolecular
mechanismsandmaternalfactors,includingthecytoskeletonandmolecular
motors that protect and enrich germ cell determinants subcellularly and
ultimatelylimitgermlinefatetojustafewcellsoftheearlyzebrafishembryo.
Once specified, by whatever mechanism, the newly specified germ cells
must retain their unique fate as they migrate through a myriad of signaling
environmentsinthegastrulatingembryototheireventualhomeinthepro-
spective gonad. As with the other transitions in the life of the germline,
maintenance of germline identity relies heavily on RNA regulation. In
Chapter7,TheresaGross-ThebingandErezRazreviewtheroleofanevo-
lutionarilyconservedRNAbindingproteininnavigatingthevoyageofthe
nascent germline to the gonad while preventing it from losing its unique
character and identity along the way.
Althoughthemechanismofgermlinespecificationcanbematernallyor
zygoticallyregulated,theinitialeventsfollowingfertilization,includingthe
early cleavages that transform the giant oocyte into the smaller cells that
makeuptheblastula,andnongermlinefatesarecompletelyundermaternal
control.However,afterjustafewcleavagecycles,theembryomustwakeup
itssleepinggenomeandbecomeanactiveplayerinitsowndevelopmentby
producingitsowngeneticresourcesandweaningitselffrommaternalcon-
trol to achieve normal development. In Chapter 8, conserved and species-
specific factors and mechanisms underlying the transition from maternal to
zygotic control are reviewed by Edlyn Wu and Nadine L. Vastenhouw.
Themechanismsthatformthescaffoldforsettinguppatternorbreaking
symmetry in the early embryo are governed by both maternal and zygotic
mechanisms.Insomespecies,thefoundationissetupbycoordinatesorspa-
tial asymmetries established in the ovary well before fertilization occurs. In
others,thefirstasymmetriesaremanifestthroughacombinationofcellular
arrangementsandgeneexpressionafterzygoticexpressionhasbegun.Inthe
thirdsectionofthisvolumethemechanismsthatpatterntheaxesofdiverse
embryosareexploredbeginningwithmaternalcontrol ofgrowth andseed
controlinfloweringplantsbyAllisonR.PhillipsandMatthewM.S.Evans
in Chapter 9. In Chapter 10, specification of the dorsal-ventral axis of sea
urchins is reviewed by Maria Dolores Molina and Thierry Lepage, and in
Chapter11,DiWuandJurrienDeanpresentmaternalcontroloftheearliest
events and fate decisions of the preimplantation mouse embryo. In
Chapter 12, Ricardo Fuentes, Mary C. Mullins, and colleagues provide
analysis of patterning in zebrafish with comparisons to patterning in other