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Copyright 0 1997 by the Genetics Society of America
Plants and the Logic of Development
m o t M. Meyerowitz
Division of Biology, California Institute of Technology, Pasadena, California 91 125
. . . plantsconstituteover 90% of theworld’s present
(and past) biomass. Thus, simply in terms of their bulk,
whatever we learn about plants has the potential to tip
thebalanceinany
debate concerning therelativefrequency of occurrence of abiological phenomenon.
NIKLA~1992
I
T seems likely that plants and animals have independently evolved multicellular development. Members
of each kingdom are composed of different types of
eukaryotic cells,implying thatthe two kingdoms diverged when theircommon eukaryotic ancestor was
unicellular and that each lineage had a considerable
unicellular history after they separated. This indicates
that each kingdom separately evolved its mechanisms
of cellular differentiation and cell-cell communication.
This in turn raises a series of questions: do land plants
and metazoans use the same fundamental mechanisms
of development and perhaps even the same genes for
similar processes, or has independent evolution of development meant theinvention of completely different
ways of doing things? Is there only one way to evolve a
developmental system, or more than one?Is more than
one type of multicellular development even possible?
The answers would reveal something of the logic of
development as a general phenomenonand would indicate the types of constraints that exist on the evolution
of development. A priori, the strongest constraints
would seem to be the starting toolkit and the fact that
any existing developmental system must be of a type
that can continue to evolve-otherwise, it would have
been competed to obscurity or extinction. The toolkits
(i.e., the startingsets offunctional genes) used by plants
and animals in their separate inventions ofdevelopment should have been similar, since both plants and
animals arose, ultimately, from the same eukaryotic lineage. That this is true is also experimentally demonstrated, as many plant and animal genes of similar function are homologous. The question then is whether the
genes used to regulate development are also homologous. If not, it is stillpossible thatnonhomologous
genes can be used for similar functions, so that the
general logicof the developmental mechanisms of
plants and animals is the same, even though theindividual gene families used for each particular function are
different. If this is the case, comparative study should
reveal the principles of development. Alternatively,
plants and animals could use completely different developmental mechanisms, in which case studying plant
development would be like finding living organisms on
Genetics 145 5-9 (January, 1997)
another planet-an opportunity tosee something completely novel. In any case, understanding the independently evolved mechanisms of development in two very
distantly related types of complex, multicellular organisms should allow a much better understanding of the
logic of development and of the interplay of chance
and necessity in the evolution of developmental mechanisms.
So, do plants and animals use the same genes for the
same developmental processes, or is everything different? Part of the answer is known, but only part. So far,
it seems that the general cellular functions of plants
and animals are homologous, but that only some of the
regulatory genes that specify organ types or cellular
domains are homologous, while others have a similar
functional logic, but use members of different families
of proteins to carry out similar functions. In one area
it seems (so far) thatplants and animals are quitedifferent-while internal cellular mechanisms are homologous, the mechanisms by which plant and animal cells
recognize their neighbors and theirenvironments seem
(at least in our currentstate of partial knowledge) strikingly different. Thus, we are beginning tofind a gradient of difference between plants and animals. At the
level of the nucleus, things look very much the same:
in plants and animals chromosomes exist and contain
highly similar histones, the chromosomes dance similarly through mitosis and meiosis, and the generaltranscriptional machinery seems very similar. When we observe the regulators of spatial patterns of gene
expression, it appears that the logic by which homeotic
selector genes and their regulators act are similar, but
the proteins that carry out comparable developmental
functions seem to be from different families. This indicates convergence on a similar type of developmental
mechanism in both kingdoms. In the cytoplasm the
gene products that carry out processes such as secretion, cellular trafficking, and biosynthesis are generally
comparable, but there arespecial processes that differentiate plants and animals-protein import in chloroplasts, for example, or muscle contraction. By the time
we are at the cell surface and consider interactions with
the outside world, the receptors for external stimuli
seem quite different, and theextracellular matrix ( k . ,
the plant cell walls, the protein matrix secreted by animal cells) is also noncomparable.
Cellular functions: The past decade and more of m e
lecular cloning of genes, and the various plant and animal genome projects, have provided a means for direct
6
E. M. Meyerowitz
comparison between the cellular functions of plants
and animals. The extensive catalogues of Arabidopsis
thaliana expressed sequence tags, e.g., reveal that this
flowering plant has homologues of animal genes involved in most housekeeping functions (NEWMAN
et al.
1994; COOKEet al. 1996). Ribosomal proteins and translation factors are similar; chaperonins arehomologous;
and ATP synthesis is mediated by homologous genes.
Glycolytic enzymes, amino acid biosynthetic enzymes,
actin, tubulin, kinesins, keratin, vacuolar sorting proteins, ubiquitin and the enzymes that act upon it, calmodulin and calmodulin-dependent kinases, and on
and on, are held in common by plants and animals.
There are of course specialized proteins that are kingdom-specific, at least so far, such as the enzymes involved in biosynthesis ofplant hormones such
as gibberellins or ethylene, or counterparts thatmake specialized
products, such as thyroid hormone, found only in animals. Some hormones are in common, though-both
plants and animals use steroid hormones, though the
exact structures of the active hormones are different,
and we have no idea if the mechanism of reception is
similar in thetwo kingdoms, as the plant receptorshave
not been characterized (CLOUSE
1996; HOOLEY1996;
LI et al. 1996; SZEKERES
et al. 1996). There are most
certainly also specialized celltypes
that distinguish
plants and animals. Plants do nothave neurons or muscles; animals do not have photosynthetic leaf mesophyll
cells, stomatal guard cells or xylem. In terms of cell
types, plants and animals are completely distinct. Even
so, the structural proteins and enzymes that make up
these very different celltypes are comparable: guard
cells andneuronsboth
use homologous potassium
channels to fulfill their functions (WARMKEand GANETZKY 1994).
Developmental regulatory proteins:The sequencing
projects and many experiments involving the cloning
of specific individual genes also show that the families
of transcription factors involved in transcriptional regulation are held in commonby plants and animals. Both
kingdoms have MADS box proteins, basic leucine zipper proteins, homeobox proteins, myb family factors,
zinc finger proteins, and so on. Functional information
on the products of individual genes allows us to begin
to see the independent evolution of plant and animal
development.
Take for exampletwo families of transcription factors
foundinboth
kingdoms: homeoboxproteins
and
MADS domain proteins. Inanimals many of the homeobox proteins act as homeotic selector genes, serving
the general function of differentiating different body
regions from each other, presumably by activating and
repressing different sets of downstream genes in different regions (MANAK and SCOTT1994). Plants also have
many homeobox genes, but so far none has been shown
to play a role in the specification of cell typein specific
spatial domains. Instead, the best-studied set of plant
homeobox genes (The K N O ~ class,
~ l KERSTEITER
et al. 1994; LINCOLN
et al. 1994) serve as activators of
cell division in different spatial domains. When animal
homeobox genes are ectopically expressed, homeotic
conversions can result (e.g., GIBSON and GEHIUNC
1988;
HALDER
et ul. 1995). Overexpression of members of the
KNOTTEDI classof plant homeobox genes activates
generalized cell division, leading to formation of new
meristems (e.g., SINHAet aZ. 1993; CHUCKet al. 1996).
In this respect, at least so far, all of the members of this
class ofhomeobox genes seem to have the same activity:
their gain of function phenotypes all seem identical.
This is not atall the case withthe fly genes, for example,
ectopic expression of the Drosophila Antennupedia gene
has utterly different effects than ectopic expression of
e y e b s . Furthermore,the animal genes arefound in
chromosomal complexes, with the order of genes related to the spatial pattern of their expression. The
plant genes are not found in complexes.
The converse situation occurs with the MADS box
genes. In this case, mutations in many of theplant
genes, or their ectopic expression, causes homeotic
conversions (e.g., MIZUKAMIand M4 1992; KRIZEK and
MEYEROWITZ
1996). This is best-studied in flowers,
where each of the four organ types (sepals, petals, stamens, and carpels) is specified by a different combination of MADS box organ identity genes, expressed in
overlapping spatial domains (WEIGEL
and MEYEROWITZ
1994). The function of theplant MADS box genes
seems to parallel the function of the animal homeobox
genes-both classes serve as homeotic selector genes
whose spatial pattern of activation determines the identity of segments, in animals, or floral whorls, in plants.
In keeping with this parallel, each of the MADS box
genes shows a different homeotic phenotype when ectopically expressed-each has functional specificity,
just as do the animal homeobox genes. So far as we
know, the animal MADS box proteins serve another
typeof function. The best-studied is serum response
factor, which is a general transcription factor that is
activated by phosphorylation of an accessory protein to
whichit binds and that serves in growth control by
regulation of @os-eventually acting in the control of
cellular proliferation, like some of the plant homeobox
genes (PRICEet al. 1996). There are other
animal MADS
box proteins also, such as MEF-2, involved in activation
of muscle cell differentiation (OLSONet al. 1995).
So we can see a strong logical parallel between the
patterns of activation, loss-of-function phenotypes, gainof-function phenotypes, and general role of the plant
MADS domain proteins and the animal homeodomain
proteins; however, the two families ofproteins are unrelated, and the founding genes of each family were almost certainly inherited in each lineage from the commonancestor. From this we can at least begin to
conclude that certain developmental functions (homeotic selector genefunctions) evolved independently
1996 GSA Medal Essay
and also perhaps that there is a necessity for this function in evolving, developing systems. Otherwise, why
would such a mechanism have arisen independently in
the only two complex multicellular lineages that we
know? There is another set of parallels, too-the plant
MADS box genes and the animal homeobox genes are
spatially regulated at thetranscriptional level, by earlieracting transcription factors. Each group of genes also
codes for transcription factors that are thought to act
by regulating downstream genes. In both plants and
animals pattern formation results from a longconversation between transcription factors, prior toany regional
differentiation. But the transcription factors used as homeotic selector genes are different.
Cell-cell and cell-environmentinterface: Develop
ment requires communication between cells and their
external environments, including neighboring cells. It
is here that differences between plants and animals
seem greatest, at least in our present state of partial
knowledge. Such differences may not be unexpected,
as the independent evolution of multicellularity in the
two kingdoms might imply that they need to have
evolved different ways of communicating from one cell
to another. However, the great differences in response
to similar environmental stimuli such as light are not
expected on this basis. Nonetheless, they exist. Little is
known about cell-cell communication in plants. One
mechanism of this communication isby
planthormones. The only plant hormone for which we have
biochemical information on the receptor is ethylene, a
gas made in plants as a response to various sorts of
stress and during ripening of some types of fruits, and
perceived by plant cells, which, depending on the cell
type, respond in a variety of ways (ECKER1995). The
ethylene receptors are two-component receptors with
clear homology to bacterial receptors of the same class,
which are histidine kinase/phosphatases and which act
through transfer of phosphates from histidines to aspartates on response regulator proteins (CHANGet al. 1993;
CHANC
and MEYEROWITZ
1994; SCHALLER
and BLEECKER
1995). In bacteria these molecules act as environmental
sensors, e.g., in chemotaxis and in oxygen and osmolarity responses (PAFWNSONand KOFOID 1992). No member of the two-component receptor class has yet been
found in animals, though there have been examples
discovered in fungi and slime molds (OTA and VARsHAVSK%' 1993; ALEX et al. 1996; SCHUSTER
et al. 1996;
WANGet al. 1996). Despite the dissimilarity ofthis plant
receptor with any known animal receptor, the closer
the pathway gets to the nucleus, the more it resembles
animal pathways. It is thought that the ethylene recep
tors communicate with a protein that resembles mammalian raf kinases, and in yeast, where more of the
downstream part of the pathway from the yeast twocomponent osmolarity receptor is known, the nextsteps
are aseries of phosphate transfers between components
of a M A P kinase cascade (MAEDA et al. 1995). MAP
7
kinases arecommon in plants aswell, thoughtheir
involvement in ethylene perception is unproven.
Animals for their part use a variety of cell surface
receptors that appear tohave no counterpart in plants.
No member of the animal receptor tyrosine kinasegene
family has been found in any plant (or in any fungus,
for that matter, HUNTER 1994). Plants do have small
GTP-binding proteins of various types, but no real ras
homologue has been found (MA 1994). No serpentine
(seven transmembranesegment)receptor
has been
found in plants, either. Plants do appear to have heterotrimeric G proteins; based on the molecular cloning of
reasonable homologues of Galpha and Gbeta
subunits
(MA 1994). But their role in the plant is generally unknown (though see below), and they do not have the
sort of diversityfound in animals: there is, for example,
only one Galpha gene known in any species of plant,
rather than the multitude
of cross-hybridizing genes
found in animals. The absence (so far, at least) of serpentine receptors, which are so often associated with
heterotrimeric G proteins in animals, indicates again
that the receptor may be different, but as the pathway
closes in on the nucleus, things become more similar.
Plants also havea large family ofapparent cell surface
receptors that have extracellular leucine-rich repeats
and that act in the cytoplasm as serine/threonine kinases ( C W G et al. 1992; WALKER1994). These LRR
kinases havebeen found to act
in perception of external
pathogens and in a variety of developmental processes
such ascelldivision
that depend on signaling from
neighboring cells ( . g . , SONG et al. 1995; TONI et al.
1996). While animals have leucine-rich repeat proteins
and serine threonine kinases, there are no known animal homologues of the large plant receptorfamily. Perhaps the plant proteins fill the role filled in animals by
receptor tyrosine kinases.
To cite one additional example, despite the fact that
plants and animals perceive and act upon light information in many ways, the receptors are completely different. Multicellular plants, like many animals, have color
vision and receptors that act at different wavelengths.
The red/far-red light receptors are phytochromes, proteins with no known homologues in animals, that use
a tetrapyrrole chromophore (QUAIL
et al. 1995). The
plant blue light receptors (cryptochromes) are flavoproteins related to bacterial photolyases (AHMAD and
CASHMORE 1996). Animal light receptors are rhodop
sins, members of the serpentine receptor family, with
a retinal chromophore; they act through heterotrimeric
G proteins (ZLJKER 1996). It is not known whether the
light pathwaysof plants and animals become similar
after thereception event, because the pathways in
plants are generally unknown. There is evidence,
though, that at least some of the processes induced by
phytochrome in plant cells require activation ofheterotrimeric G proteins (NEUHAUSet al. 1993), just as do
processes activated by rhodopsins in animal cells. There
8
E. M.Meyerowitz
are also early indications that proteins in one protein
complex involved downstream of phytochrome have
counterparts in mammals, but they are not proteins
known to be involved in animal photoreception (CHAMOVITZ and DENG1995).
The extracellular matrix of plant and animal cells
is also completely different, plants having a cellulose/
hemicellulose cell wall that binds neighboring cells to
each other; while animals rely on proteins for their
extracellular matrix. Plant cell walls have proteins such
as the various arabinogalactan proteins, and expansins
(COSGROVE
1996; KREUGER and VAN HOLST1996).
These are not related to animal extracellular matrix
proteins. Thus, extracellular matrices and transmembrane receptors, even though they may serve similar
functions in terms of development and cellular communication, appear tohave evolvedfrom different starting
points and by use of different families of proteins.
Conclusions: In our current state of partial knowledge, it appears that there is a gradient of difference
between plants and animals, from quite similar in
housekeeping processes in nucleus and cytoplasm, to
logically similar but biochemically distinct regulatory
aspects ofdevelopment and control of cellular differentiation, to utterly distinct means of communicating
from each cell to its neighbors and to theoutside world.
This view results in part from ignorance, though. The
discovery of a set of animal homeotic selector genes
that areMADS domain proteins,of an animal two-component receptor, or of a plant serpentine receptorand
tyrosine kinase wouldchange it. Nonetheless, it is worth
keeping a running score. If we accept thata comparison
of the two independently evolved mechanisms of complex multicellular development allows us to differentiate those aspects of developmental biology that arenecessary for anyevolved developing system from those
that are only accidental, we can pointto long conversations between transcription factors as being necessary
for pattern formation and to cell-cell communication
as being necessary for functional multicellularity. An
additional take home lesson is that we need to learn
more about both plant andanimal development to be
certain that these lessons are true and to learn about
additional logically parallel systems that use unrelated
gene products. In particular we must understand the
full array of mechanisms used in genetic regulation in
both kingdoms and the nature of the molecules involved in cell-cell communication and environmental
response. There areseveral paths to this understanding.
One is to continue the successful application of developmental genetics to both plants and animals, starting
with mutations that affect critical developmental functions and proceeding via genetics, molecular genetics,
and biochemistry to an understanding of the actions of
the proteinsand protein complexes that actto regulate
differentiation, pattern formation,and cellular communication. Another is comparative genomics, to letus see
if we have completed the job of understanding each
species under study and to allow complete comparisons
of gene numbers, gene homologies, and the genetic
complements of as wide an array of organisms as possible (GABORMIKLOSand RUBIN1996). Comparisons of
plants and animals will be an important part of this,
but it should also be noted that a real comparison of
plants and animals will also require knowledge of the
starting toolkit of genes that was commonly inherited
by both lineages. This means taking a careful look at
prokaryotic genomes and also at those of a variety of
unicellular eukaryotes. With this information we can
also begin to come to an understanding of the evolutionary origin of the proteins used in developmental
regulation and cellular communication and come to
grips with the question of the origin of evolutionary
novelties.
To emphasize the importance of the broadest possible comparative approach to an understandingof development, consider an experiment to find out whether
there is indeed a limited set of waysthat complex multicellular development can evolve from identical unicellular organisms. The experiment would be to take a
series of identical cells and place them in conditions
that favor multicellularity and then to wait for two billion years and observe the result. One would expect the
result to be highly revealing, to lead to a new appreciation for the evolution of development, and to point
the way to new ways of thinking about ontogeny. This
experiment is difficult to perform: among other things,
the less-than-two billion year length of funding cycles,
as well as the limited willingness of many students and
postdocs to take on such long-term projects, are serious
impediments. Fortunately, nature has performed this
experiment for us with plants and animals. While the
starting cells were not identical, they were descended
from a common ancestor; and while the conditions of
evolution in the two lineages were disparate, a full understanding of development in the two kingdoms will
give us information and food for thought that studies
in only a single kingdom will not.
My laboratory’s work on plant genetics and plant developmental
biology is supported by the U.S. National Science Foundation (MCB
9204839), National Institutesof Health (GM45697), and the Department of Energy (FG03-88ER13873).
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