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Plant Embuyogenesis: Zygote to Seed Authou(S) 3ODQW(PEU\RJHQHVLV=\JRWHWR6HHG $XWKRU V 5REHUW%*ROGEHUJ*HQDURGH3DLYDDQG5DPLQ<DGHJDUL 6RXUFH6FLHQFH1HZ6HULHV9RO1R 2FW SS 3XEOLVKHGE\$PHULFDQ$VVRFLDWLRQIRUWKH$GYDQFHPHQWRI6FLHQFH 6WDEOH85/http://www.jstor.org/stable/2885440 . $FFHVVHG Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Association for the Advancement of Science is collaborating with JSTOR to digitize, preserve and extend access to Science. http://www.jstor.org This content downloaded from 164.67.109.135 on Fri, 18 Jul 2014 20:08:48 PM All use subject to JSTOR Terms and Conditions m.......... ARTICLES Most morphogeneticevents in flowering Plant Embryogenesis: plants occur in the postembryonicsporo- phyte after seed germination(Fig. 1) (2). Vegetativeorgan systems differentiate con- Zygote to Seed tinuouslyfrom root and shoot meristematic regionsthat are formedinitially during em- Robert B. Goldberg,*Genaro de Paiva, RaminYadegari bryogenesis.The reproductiveorgans of the flower are differentiated from a repro- Mostdifferentiation events in higherplants occur continuouslyin the postembryonicadult grammedshoot meristemafter the seedling phase of the life cycle. Embryogenesisin plants, therefore, is concerned primarilywith has become a matureplant (Fig. 1) (25). establishing the basic shoot-root body patternof the plant and accumulatingfood re- Thus, a germlineanalogous to that foundin serves that willbe used by the germinatingseedling aftera periodof embryonicdormancy animals (1) is not set aside during plant withinthe seed. Recent genetics studies inArabidopsis have identifiedgenes that provide embryogenesis. new insightinto how embryos formduring plant development. These studies, and others A matureflowering plant embryocon- using molecularapproaches, are beginningto revealthe underlyingprocesses that control tains two primaryorgan systems-the axis plant embryogenesis. and cotyledon (Fig. 1) (2). These organs have distinct developmentalfates and are both composedof threebasic, or primordial, tissue layers-protoderm,procambium, and A majorproblem in plant developmentis lecularapproaches suggest that a plant em- groundmeristem-which will become the to unravelthe mechanismsoperating dur- bryohas a modularstructure and consistsof epidermal,vascular, and parenchymatissues ing embryogenesisthat enable a plant to severalregions that formautonomously dur- of the youngseedling, respectively (2). The specifyits body plan and tissue differentia- ing embryogenesis. axis, or hypocotyl-radicleregion of the em- tion patterns.Although progresswith a va- bryo,contains the shoot and root meristems rietyof animalsystems has been spectacular Embryos Begin the Diploid Phase and will give rise to the matureplant after in this regard(1), a detailedunderstanding of the Higher Plant Life Cycle seed germination(Fig. 1). By contrast,the of the events that govern plant embryo cotyledon is a terminallydifferentiated or- formationhas yet to be realized.One obsta- The flowering plant life cycle is divided gan that accumulatesfood reservesthat are cle in achievingthis goal is the location of into haploid and diploid generationsthat utilizedby the seedlingfor growthand de- embryoswithin the plant and their relative are dependent on each other (Fig. 1) (2, velopmentbefore it becomesphotosynthet- inaccessibilityto experimental manipula- 16-18). The haploid, or gametophytic, ically active (Fig. 1). The cotyledon func- tion, particularlyat the early stagesof em- generationbegins after meiosis with spores tions primarilyduring seed germinationand bryogenesis.In floweringplants, reproduc- that undergomitosis and differentiateinto senesces shortly after the seedling emerges tive processesoccur within floral organs either a pollen grain(male gametophyte)or from the soil. Embryogenesisin higher (Fig. 1) (2). The egg cell is present in the an embryo sac (female gametophyte) (3, plants, therefore,serves (i) to specifymeri- ovule, a multicellularstructure that is buried 19-20). The pollen grain contains two stems and the shoot-root plant body pat- beneath severalcell layersof the pistil, the sperm cells, whereasthe embryosac con- tern, (ii) to differentiatethe primaryplant female reproductiveorgan (2-4). Because tains a single egg (Fig. 1). Other accessory tissue types, (iii) to generate a specialized egg cell formation,fertilization, and embry- cells within the haploid male and female storageorgan essential for seed germination ogenesisoccur within the pistil, it has been gametophyteshelp facilitatethe pollination and seedling development,and (iv) to en- difficultto dissectthe majorevents that take and fertilizationprocesses (3, 19, 20). The able the sporophyteto lie dormant until placeduring the earlystages of higherplant male and female gametophytesare derived conditions are favorablefor postembryonic development. from specializedspore-forming cells within development. Recently, it has become feasible to iso- the reproductiveorgans of the flower(3, 4, late plant eggs and fertilizethem in vitro in 21). By contrast, the diploid, or sporo- The Shoot-Root Body Plan Is order to investigate the initial events of phytic, generationbegins after fertilization Generated During Early planteribryogenesis (5). In addition,genet- with the zygoteand formsthe matureplant Embryogenesis ic approacheshave been used to identify with vegetative organs (leaf, stem, root) genes requiredfor variousembryogenic pro- and flowers that contain the reproductive How the embryoacquires its three-dimen- cesses, includingpattern formation(6, 7). organs(anther and pistil) (Fig. 1). sional shape with specializedorgans and Genetic manipulationof Arabidopsisthali- Two fertilizationevents occur in flower- tissues,and what gene networksorchestrate ana, by both chemical mutagenesis(8-12) ing plants (2, 22). One spermunites with embryonicdevelopment remain majorun- and insertionalmutagenesis (13-15), has the egg cell to producea zygoteand initiate resolvedproblems. From a descriptivepoint identified a large numberof mutants that embryogenesis.The other uniteswith a spe- of view, plant embryogenesiscan be divided are blocked at differentstages of embryo- cializedcell within the embryosac (central into three generalphases in which distinct genesis.In this reviewwe outline the major cell) to initiate the differentiationof the developmentaland physiologicalevents oc- insightsthat have been derivedfrom studies endosperm,a triploidtissue that is neither cur: (i) postfertilization-proembryo,(ii) of Arabidopsisembryo mutants, and we sum- gametophyticnor sporophyticin origin(Fig. globular-hearttransition, and (iii) organex- marize gene transcriptionexperiments in 1) (23). The endospermis present during pansion and maturation(26-28) (Fig. 2 other plants that providenew information seed developmentand providesnutrients for and Table 1). Although there is consider- about the processesregulating higher plant eitherthe developingembryo, the germinat- able variationin how embryosin different embryogenesis.Both the genetic and mo- ing seedling,or both (23). Fertilizationalso plant taxa form (29), the overalltrends are causesthe ovule, containingthe embryoand remarkablysimilar (29). We summarizethe Authors are in the Department of Biology, University of endosperm,to develop into a seed and the Capsella and Arabidopsispattern of embryo California,Los Angeles, CA 90024-1606, USA. ovary to differentiateinto a fruit, which development (29-33) because (i) it is one *To whom correspondence should be addressed. facilitatesseed dispersal(Fig. 1) (24). of the most well-studied forms of plant em- SCIENCE * VOL.266 * 28 OCTOBER1994 605 This content downloaded from 164.67.109.135 on Fri, 18 Jul 2014 20:08:48 PM All use subject to JSTOR Terms and Conditions Fig. 1. The life cycle of a 1 Pollen flowering plant with em- Egg cell formation, grains phasis and fertilization on egg cell forma- pollination, Stigma permcells tion and seed develop- -ube ment. [Adapted from (16, Pistil Megaspore Surviving Embryo Female Style nucleus 26).J mothercell megaspore sac gametophyte(n) Male (2n) (n) \p ntipodal gametoht Nucellus CCentral cells gametophyte / > n~~~~Meiosis M itosis { cell XO (nr)fri - Me~~~~~~~sis F~~~~~~~~J~~~~ ~ Ovary-fruit Ovule rynergid Flower Flower Petal Funiculus Integuments ~~~~Egg cells ~ 1I ~~~~~~~~~~~~~~~~~~~~~cell - Anther Micropyle // Pistil epal Germinating Dormant Developing Fertilizedendosperm Seedling seed seed seed nucle s (3n) aotyledo tyldo Endosperm LShootmeristemI11 1 ootmeristem Root FFAA Embryo Developing egg (2n) CotyledonsJ embryo Seed developmentand germination bryogenesis,dating back to the classical the suspensor(Fig. 2). In Arabidopsis,the to be passedfrom the maternalsporophyte studiesof Hanstein,Schaffner, and Soueges suspensorcontains only 7 to 10 cells (Fig. into the developing proembryo(Fig. 2) with Capsella(30-32), (ii) it has an invari- 2). The suspensoranchors the embryoprop- (35). The suspensorsenesces after the heart ant divisionpattem duringthe earlystages, er to the surroundingembryo sac and ovule stage and is not a functional part of the which allows cell lineagesto be tracedhis-
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