Plant Physiol. (1 996) 11 2: 5-1 O

Sizing Up the Floral Meristem’

Detlef Weigel* and Steven E. Clark

Plant Biology Laboratory, Salk lnstitute for Biological Studies, 1001 O North Torrey Pines Road, La Jolla, California 92037 (D.W.); and Department of Biology, University of Michigan, 830 University Avenue,

Ann Arbor, Michigan 481 O9 (S.E.C.)

About 200 years ago, the poet and naturalist Goethe (1790) suggested that flowers were modified shoots and floral organs were modified leaves. In 1991, this assertion was spectacularly confirmed by Bowman et al., who showed that they could transform the sepals, petals, sta- mens, and carpels of Arabidopsis flowers into leaf-like organs simply by eliminating a set of three floral regulatory genes, AGAMOUS (AG), PISTILLATA (PI), and APETALA2 (AP2). At first it might seem surprising that flowers and shoots are homologous structures, especially when one thinks of such extremes as the tiny flowers of duckweed, barely visible to the naked eye, and the trunk of a mature tree, which can be tens or even hundreds of feet tall. It becomes a little less mysterious if one looks at the earliest stages of development, when flowers or shoots start to arise. Both types of structures are formed from collections of stem cells, termed meristems, which have an organiza- tion that is very similar for both flowers and shoots, with at least three domains that can be distinguished by histolog- ical and experimental criteria. The central zone, in which cells remain undifferentiated, serves as a stem cell pool for the renewal of the meristem. Surrounding this is the pe- ripheral zone, where new organs are initiated. Underlying the central zone is the rib meristem, which forms the bulk of the interior tissue (Fig. 1). Starting with this common structure, shoot meristems produce leaves with associated axillary shoots and flowers, whereas flower meristems give rise to floral organs such as sepals, petals, stamens, and carpels. Apart from the differences in the types of organs they produce, shoot and flower meristems often differ in phyllotaxis, which is the pattern with which these organs are produced, and in determinacy, which is whether a meristem is consumed in the production of a terminal structure.

Given the similarities between flower and shoot meri- stems, as well as the obvious differences in their subse- quent development, one would expect to find at least two classes of genes to be active in early shoot and flower meristems: one class that controls the structural features

Research in our laboratories is supported by the National Science Foundation (NSF), the U.S. Department of Agriculture, and the Samuel Roberts Noble Foundation. D.W. is an NSF Young Investigator.

* Corresponding author; e-mail Detlef-Weigel@qm.salk.edu; fax 1-619-558-6379.

5

common to both types of meristems and another class that discriminates between the two types. Both classes of genes have been identified: genes in the first class are called meristem-structure genes and members of the second class are commonly known as meristem-identity genes. Genes in the latter category in turn regulate other factors that elab- orate the species-specific differences between shoot and flower meristems. We review here recent progress made in the understanding of these different classes of genes.

BUlLDlNG AND MAlNTAlNlNC A MERISTEM

The apical shoot meristem forms during embryogenesis, a process that is disrupted in several Arabidopsis mutants, including shoot meristemless (stm), wuschel (wus), zwille ( z l l ) , and pinhead (pnh), a11 of which either lack entirely or have a severely reduced shoot meristem (Barton and Poethig, 1993; Jürgens et al., 1994; McConnell and Barton, 1995; Clark et al., 1996; Laux et al., 1996). In contrast, an enlarged shoot meristem is caused by mutations in the CLAVATA (CLV) genes (Leyser and Furner, 1992; Clark et al., 1993, 1995). Of a11 these genes, only ZLL and PNH activities are largely specific to the embryo. The others affect not only the postembryonic development of the apical shoot meri- stem, but also the lateral shoot meristems that form in the axils of leaves produced by the apical shoot meristem and the flower meristems produced by the shoot meristem after floral induction (Fig. 2) . The effects on the different types of meristems are similar or identical for each mutation, such that a11 meristems are either reduced or enlarged. The deviations from normal meristem size and organization are specific, which is particularly obvious from the floral phe- notypes. Regardless of whether a mutation reduces or in- creases the number of floral organs, the number of sepals, the outermost organs, is least affected, whereas the number of carpels, the central organs, is most strongly affected, suggesting that these genes control either the establishment or the maintenance of the central zone of the meristem.

Having several mutations that affect the same develop- mental process at hand, one can question the relationships between these genes by analyzing double mutants involv- ing either mutations that have the same effect on meristem development or mutations that have opposite effects. For example, the phenotype of double mutants carrying strong clvl and clv3 alleles is identical to that of either single mutant, suggesting that the two genes act in the same

Weigel and Clark Plant Physiol. Vol. 112, 1996

Figure 1. A, Florally induced shoot apex ol Arabidopsis thaliana as seen in the scanning electron microscope. White line indicatesapproximate plane of section for the schematic cross-section shown in B. Flower anlagen and primordia are indicated by shading.Note how these groups of cells are displaced toward the periphery. CZ, Central zone; PZ, peripheral zone; RM, rib meristem.

pathway (Clark et al, 1995). Important information hasalso come from the study of double mutants involving civand stm or wus alleles. Although the single-mutant pheno-type of the weak stm-2 allele and wus are similar, eachinteracts with civ mutations in a very different manner; wusmutations are epistatic to clvl and double-mutant flowersshow only the wus phenotype (Laux et al., 1996). Oneexplanation is that CLV1 negatively regulates WUS andthat the clvl phenotype results from WUS hyperactivity.Alternatively, WUS might be required for central meristemidentity and CLV1 could act within the central zone that isset up by WUS activity. Since this zone fails to form in wusmutants, clvl mutations would have no effect in double-mutant plants.

In contrast to the epistatic interactions between wus andclvl mutations, stm and civ suppress each other's defects(Clark et al., 1996). It appears that STM and CLV act com-petitively to regulate meristem size, such that it is possibleto compensate for loss of function in one pathway byreducing or eliminating activity of the other pathway. It is

developmental time

shoot meristemestablishment

shoot meristemmaintenance

flower meristemmaintenance

PNH, ZLL

STM, WUS

CLV1, 2, 3

AG, APS,PI, SUP

Figure 2. Temporal action of genes that control meristem structure.

unlikely that this reflects direct interaction between the twogenes, since a civ mutation can partially suppress a pre-sumed null allele of stm. They are more likely acting on acommon target, thereby ensuring the proper balance ofmeristem renewal and differentiation. The restoration ofmeristem function in the civ stm double mutant shows thatSTM is not absolutely required for meristem function,which begs the question of why a plant needs the activitiesof genes such as STM and CLV at all. The answer comesfrom the double-mutant phenotype: Although stm civplants form meristems, the meristems fail to maintain theirproper size and can become either too large or too small,showing that STM and CLV have important roles in thehomeostasis of meristem size.

In addition to maintaining shoot meristems, severalSTM-related factors can also function in the de novo initi-ation of meristems. STM belongs to a class of genes that allencode homeodomain proteins and that are predominantlyexpressed in shoot and flower meristems (Long et al.,1996). Several members of this gene family, the prototypeof which is the KNOTTED (KN) gene of maize, can induceectopic shoots when they are ubiquitously expressed(Sinha et al., 1993; Lincoln et al., 1994). Given the extensivesimilarities in structure and expression pattern of KN andSTM, which might even be orthologs (Long et al., 1996), itis not unlikely that the shoot-meristem-inducing activity isshared by STM.

ASSIGNING FLOWER-MERISTEM IDENTITY

Although wus, stm, and civ mutations affect both shootand flower meristems, which confirms that these two mer-istem types are structurally similar, each type of meristem

Sizing Up the Floral Meristem 7

forms organs in distinct ways. Apart from the differences in the organs produced, there are notable differences in the patterns of organ emergence-spiral versus concen- tric-and in the maintenance of the central zone. Shoot meristems of wild-type Arabidopsis are indeterminate and continue to produce new organs throughout the life of the plant, whereas flower meristems are determinate and are consumed in the formation of a defined number of floral organs. Recent experiments have shown that flower-specific growth patterns can be initiated by a single meristem-identity gene.

Meristem-identity genes were first identified through loss-of-function mutations that cause either complete or partia1 conversions of flowers into shoots. In Antirvhinum plants mutant for FLOXICAULA (FLO) or Arabidopsis plants mutant for the orthologous gene LEAFY (LFY), flow- ers are replaced by shoots. Floral structures can eventually develop in either mutant, albeit rarely inflo mutants, indi- cating that FLOILFY activity is not absolutely required for a11 aspects of flower development (Schultz and Haughn, 1991; Carpenter et al., 1995). This is at least partially due to the overlapping action of another gene, SQUAMOSA (SQUA) in Antirrhinum and APETALAZ (APZ) in Arabidop- sis (Huala and Sussex, 1992; Weigel et al., 1992; Carpenter et al., 1995). Although expression of FLOILFY and SQUAI APZ can be established independently of each other, the activity of either gene alone is obviously not sufficient to initiate normal flowers. Therefore, it has been unclear until recently whether either gene would be sufficient to initiate normal flower development in an otherwise wild-type background. This question has been answered by the con- struction of transgenic plants in which LFY or APZ is under the control of a constitutively active vira1 promoter (35S::LFY, 35S::APZ), such that they are expressed through- out a11 plant tissues including shoot meristems. In these transgenic plants, ectopic flowers, which are largely nor- mal in terms of the identity and arrangement of floral organs, develop in positions where shoots are found in wild type (Mande1 and Yanofsky, 199513; Weigel and Nils- son, 1995). Normal flower development in transgenic plants with ectopic LFY or AP1 expression is still depen- dent on the presence of the other gene, such that 35S::LFY apZ flowers have defects typical of apZ (secondary flowers, reduced number of petals, transformation of sepals into leaf-like structures) and 35S::API l fy flowers have defects typical of l f y (absence of petals and stamens, spiral phyl- lotaxis). These observations indicate that either gene can induce activity of the other in ectopic positions and that the formation of normal flowers results from the combined activity of both genes.

ORCAN PATTERNINC A N D DETERMINACY W l T H l N FLOWERS

One of the most well-understood consequences of flower- meristem determination is the induction of a set of floral homeotic genes that are responsible for conferring specific organ identities, although it is still unclear how this is achieved at the molecular level. However, two other as- pects of flower meristem development are equally impor-

tant, namely, the limitation of cell proliferation in the cen- tral zone and the switch from spiral to whorled phyllotaxis. A detailed study of how Antirrhinum meristem-identity genes might control this difference in phyllotaxis has re- cently been undertaken by Carpenter et al. (1995). They found that the initial appearance of a newly formed lateral meristem is the same in wild-type flo and squa plants well after the expression of FLO or SQUA transcripts is first detected in flower meristems of wild-type plants. Among these three types of meristems, those of wild type are the first to change their shape from rectangular to pentagonal, with five sepal primordia eventually emerging from the five sides of the pentagon. New organ primordia arise at the same time in flo mutants but without a preceding change in meristem shape, and instead of five sepal pri- mordia, only two bract primordia are formed opposite of each other in lateral positions. The central meristem inflo mutants continues to grow and the next three bract pri- mordia arise delayed, initiating a phyllotactic spiral. The development of flower meristems in squa mutants is similar to that of flo mutants in that two lateral bract primordia initially emerge, but the subsequent primordia arise sooner than in flo mutants. In addition, the position of these bract primordia is closer to the position of the (whorled) sepal primordia of wild type. These observations suggest that the timing of primordia initiation or the rate of proliferation of the flower meristems, or a combination of both, is impor- tant for the differences seen in the phyllotaxis of flowers and shoots.

These findings imply that meristem-identity genes acti- vate a set of genes that specifically regulate the structure of the flower meristem. This is borne out by the observation that the structure of flower meristems is not only under the control of general regulators, including the above de- scribed genes CLV, STM, and WUS, but that there are additional genes that act only in flower meristems. Among these, severa1 have dual functions in controlling organ identity and cell proliferation in the young flower. Most of the genes in this class have been cloned, and their expres- sion is dependent on the activity of the meristem-identity genes (Weigel and Meyerowitz, 1993; Hantke et al., 1995). In addition to the organ-identity genes AG, Pl, and APETALAS (AP3), two Arabidopsis genes that specifically regulate floral organ number have been studied in detail: SUPERMAN (SUP) and PERIANTHIA (PAN). The effects that these genes have on cell division are independent of the CLVIWUSISTM network, and double mutants have phenotypes that can be interpreted as being mostly addi- tive (Bowman et al., 1992; Clark et al., 1993; Laux et al., 1996).

A particularly dramatic effect on organ number is seen in the flowers of plants that are mutant for the AG gene of Arabidopsis or its Antirrhinum ortholog PLENA. These genes are not only positive regulators of stamen and carpel identity but are also required for meristem determinacy (Bowman et al., 1991; Bradley et al., 1993). In mutant flow- ers, the center of the flower meristem is not consumed in the formation of carpels but continues to produce flowers within flowers, thus giving rise to an indeterminate flower

8 Weigel and Clark Plant Physiol. Vol. 11 2, 1996

meristem similar to the indeterminate shoot meristem. This function in meristem determinacy can be separated from AG‘s role in controlling organ identity (Sieburth et al., 1995).

Two other organ-identity genes that control cell division within the flower are AP3 and PI. Ectopic expression of these genes causes additional whorls of stamens to form in the center of the flower (Jack et al., 1994; Krizek and Mey- erowitz, 1996), whereas ap3 or pi loss-of-function mutants have reduced numbers of third-whorl organs (Bowman et al., 1991; Jack et al., 1992). Similarly, ectopic expression of AG in ap2 mutants leads to reduced AP3 and PI expression, thereby causing a reduction in organ number in the outer whorls (Bowman et al., 1991; Jack et al., 1992; Goto and Meyerowitz, 1994).

The function of AP3 and PI as positive regulators of cell division are counteracted by a gene with an expression dependent on AP3 and PI activity. This gene, SUP, is normally expressed at the boundary of the third and fourth whorl, and its inactivation leads to the formation of addi- tional stamens (Schultz et al., 1991; Bowman et al., 1992). This effect is similar to what is seen in transgenic plants with ectopic AP3, or AP3 and PI, expression (Jack et al., 1994; Krizek and Meyerowitz, 1996). The function of SUP as an APSIPI antagonist becomes particularly obvious when a sup mutation is introduced into transgenic plants in which AP3 and PI are constitutively expressed, resulting in a completely indeterminate flower meristem (Krizek and Meyerowitz, 1996). A surprising finding is that SUP has apparently nonautonomous effects as the proliferation of fourth-whorl cells, which are adjacent to SUP-expressing cells in wild type, is reduced in sup mutants. This suggests that the SUP-expressing boundary cells have special prop- erties, which possibly correlates with observations made by Vincent et al. (1995), who found that cells at the bound- ary of floral organs proliferate at a different rate than those in the center.

Another gene that antagonizes SUP in regulating AP3 and PI is UNUSUAL FLORAL OXGANS (UFO) (Levin and Meyerowitz, 1995; Wilkinson and Haughn, 1995). In ufo mutants, AP3 and PI activity is reduced, making ufo flow- ers similar in phenotype to those of weak ap3 and pi alleles, with a few petals and stamens still being present. ufo and sup mutations partially suppress each other, suggesting that the products of these genes affect common processes. It is not very likely that they interact directly, since their expression patterns do not appear to overlap (Ingram et al., 1995; Sakai et al., 1995). An additional trait that UFO shares with AP3, PI, and SUP is that it also affects cell prolifera- tion in the flower meristem, which is revealed through double mutants with ag, in which the flower meristem overproliferates and fasciates, a phenotype similar to the one seen in ag sup double mutants (Bowman et al., 1992). In contrast to the effects on AP3 and PI activity, the effects of sup and ufo mutations in an ag background go in the same direction, with the triple mutant showing even more severe defects, indicating that UFO and SUP control cell prolifer- ation through independent mechanisms (Levin and Mey- erowitz, 1995).

ORGAN SPACINC AND FLOWER SYMMETRY

In contrast to the previous mutations, which change floral organ number through their effects on cell division in the flower meristem, pan mutations alter the spacing of organ initiation without noticeably increasing the size of the flower meristem (Running and Meyerowitz, 1996). Species of the mustard family Brassicaceae, of which Arabidopsis is a member, have the common feature of tetramerous flowers, with four organs per perianth whorl (the only exception being the complete absence of petals in a few genera) (Endress, 1992). In pan mutants, the moda1 flower organ number is five in the outer three whorls, making it identical to the many species with pentamerous flowers (Running and Meyerowitz, 1996). Another Arabidopsis mutant has been found that has a phenotype similar to pan, with approximately five sepals and five petals per flower, but that mutant also shows an increase in flower-meristem size at early stages, indicat- ing that the effect of pan mutations on organ spacing is very specific (Running and Meyerowitz, 1996). As ex- pected for a gene that specifically regulates organ spac- ing, PAN acts downstream of meristem-identity genes but independently of organ-identity genes, as inferred from the analysis of relevant double mutants.

Because there are four media1 and two lateral stamens, flowers of Arabidopsis are normally considered disymmet- ric, having two planes of symmetry. During development, however, Arabidopsis flowers appear bilaterally symmet- ric because the abaxial sepal arises first. This subtle asym- metry during early development is retained in pan mutants but not in other mutants with defects in floral organ num- ber, again confirming the specific effects of pan on organ spacing as opposed to meristem growth.

The irregular or zygomorphic organization of floral or- gans, which is thought to be an evolutionarily advanced condition, is far clearer in many plant species other than Arabidopsis. Two of the most obvious features of this irregularity are position-dependent differences in petal and stamen development. In Antirrhinum, severa1 genes with overlapping function, including the CYCLOIDEA (CYC) gene, are required for zygomorphic development (Coen et al., 1995). Based on position and organ shape, one can distinguish two dorsal petals, two side petals, and a ventral petal in Antivrkinum flowers. Furthermore, of the five sta- mens that are initiated in alternate positions with and interior to the petals, the dorsal one is aborted and the two side stamens are shorter than the ventral ones. cyc mutants have much more regular flowers, giving rise in the most extreme cases to flowers with five-fold symmetry, all po- sitions being occupied by “ventral” organs. cyc mutations can also affect organ number by sometimes producing six sepals and petals instead of the normal five (Carpenter and Coen, 1990). Whether this indicates a fundamental similar- ity between PAN and CYC genes remains to be seen.

-

PERSPECTIVES

We have presented here a simple view of the flower meristem in which its organization is controlled by general

Sizing Up the Floral Meristem 9

regulators that also act in shoot meristems, as well as by flower-specific regulators that are under the positive con- trol of the early-acting meristem-identity genes (Figs. 2 and 3). The reality is more complex, however, which can be deduced from the genetic interactions between meristem- structure and meristem-identity genes or from more gen- eral considerations. For example, LFY and APZ are ex- pressed very early in the incipient flower meristems. These in turn are produced by the shoot meristem, in which establishment and maintenance are regulated by the meristem-structure genes. Conversely, LFY and AP1 are required to modulate the activity of meristem-structure genes to limit proliferation of the central zone in flower meristem. Such changes in the activity of meristem- structure genes have been directly observed through the different expression patterns of the recently cloned STM gene in shoot and flower meristems (Long et al., 1996).

This complex, interlocking gene hierarchy may explain some of the idiosyncratic interactions seen in multiple mu- tants defective in genes controlling both meristem struc- ture and identity, of which the l f y clvl double mutant is an interesting example (Clark et al., 1993). On the one hand, the overproliferation of the shoot meristem caused by clvl mutations is enhanced by loss of LFY activity. Although defects in cell proliferation are observed in l f y single mu- tants, these are normally the opposite of the overprolifera- tion seen in clvl mutants, such that flowers and their subtending bracts are often aborted or much reduced (Wei- gel et al., 1992). Thus, the effects seen in l jy clvl double mutants do not simply result from additive interactions of l f y and clvl. Rather, it appears that LFY normally partially compensates for the cell differentiation defect of clvl mu- tants. On the other hand, the flower-to-shoot conversion seen in l f y a p l double mutants is further enhanced by clvl, such that triple mutants have an even lower incidence of floral structures than the l f y a p l double mutant, indicating that CLVl can affect not only meristem structure but also meristem identity (Clark et al., 1993). A phenotypic en- hancement is also seen in wus a p l double mutants. Al- though the outer whorls are almost normal in wus flowers, most wus a p l flowers develop no floral organs at all (Laux et al., 1996). We do not know whether the synergistic effects seen in double mutants reflect overlapping func- tions of the wild-type gene products or regulatory interac- tions in complex, not clearly understood ways. Alterna- tively, certain mutant backgrounds might result in floral

Meristem Structure wus ,\

I - Flower-Meristem ldentity

LFV, AP1

Structure Spacing ldentity Flower-Meristem Floral Organ Floral Organ

AG, AP3, Pl, SUP PAN

Growth and Cell ~ i ~ i ~ i ~ ~

CDC2, CVCLINs?

Figure 3. Proposed interactions between genes controlling meristem structure and identity.

fate being unstably specified, such that disruption of yet another genetic pathway results in insufficient develop- mental information to proceed with a flower-specific program.

Finally, we have so far ignored the fact that the shoot meristem itself undergoes phase changes during develop- ment. One prominent example of a phase change is the switch from decussate (leaves opposite each other) to spiral phyllotaxis in the apical shoot meristem of Antirrhinum. Although this change normally coincides with the switch from the production of lateral shoot meristems to flower meristems, any causal relationship between these two changes is unknown. However, several genes with an ex- pression pattern in the shoot meristem that changes upon floral induction have been identified. One example is the STM homolog KNAT1, in which expression in the shoot meristem is lost during the transition to flowering (Lincoln et al., 1994). The opposite effect is observed with two recently discovered genes of the Arabidopsis relative Sina- pis alba. RNAs of these two genes, called SaMADS A and SaMADS B, start to accumulate rapidly and specifically in the shoot apical meristem in response to photoperiodic treatments that induce flowering (Menzel et al., 1996). Both genes encode MADS domain proteins and are thus similar in structure to many of the known floral regulatory genes. An apparent ortholog of one of these genes has been cloned from Arabidopsis (Mande1 and Yanofsky, 1995a). Unfortu- nately, the map position of this gene, AGL8, does not coincide with the location of any known mutation affecting shoot or flower development. It is possible, however, that AGL8 acts redundantly with the presumed Arabidopsis ortholog of the SaMADS A gene and that a mutant pheno- type requires the simultaneous elimination of both genes. Reverse genetic approaches could be useful to solve such questions.

In this review we have shown how poorly we under- stand the interactions between the different genes that regulate various aspects of meristem structure and behav- ior, but we are optimistic that this will rapidly change, since several of the genes controlling shoot and flower meristem development have been cloned and many more are likely to be isolated in the near future. The next step will be to understand how these genes interact with the mechanisms controlling growth and cell division to pro- duce the different patterns of organs produced by meri- stems. Once we have learned how model species such as Antirrhinum and Arabidopsis size up flower meristems, we can then turn to other questions, such as how the vast diversity of meristem size and behavior found throughout the flowering plants is generated.

ACKNOWLEDGMENTS

We thank Beth Krizek, Thomas Laux, Siegbert Melzer, Elliot Meyerowitz, and Mark Running for sending preprints and Don Fosket, Igor Kardailsky, Thomas Laux, and Marty Yanofsky for discussion.

Received February 20, 1996; accepted April 10, 1996. Copyright Clearance Center: 0032-0889 /96/ 112/0005 / 06.

10 Weigel and Clark Plant Physiol. Vol. 112, 1996

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