Plant Physiol, January 2001, Vol. 125, pp. 112-114
Plant Cell Identity. The Role of Position and Lineage
Ben
Scheres*
Department of Molecular Cell Biology, Utrecht University, Padualaan
8, 3584 CH Utrecht, The Netherlands
 |
INTRODUCTION |
Cells in multicellular organisms
acquire different identities in an ordered spatial arrangement. How do
cells learn about their identity? The first three-quarters of the past
century provided essentially two different explanations. On the one
hand, descriptions of reproducible cell lineage and surgical
experiments indicated that some cells only give rise to one particular
progeny. These findings suggested that cell fate was restricted early
in development and that cells passed on this decision to their progeny:
a lineage-based mechanism (Fig. 1A). On
the other hand, cell fate was not always correlated with lineage and
many cells in developing organisms changed their fate in a new spatial
context even at late stages of development: a position-based mechanism
(Fig. 1B). Hence, two concepts of pattern formation emerged in
which ancestral or neighboring cells determine the fate of a given
cell. This review attempts to examine how these two concepts became
substantiated over the past 25 years. A short account like this can
only be incomplete and personally biased, but may still serve as a
primer for the interested reader to make her/his own historical
reconstruction.
View larger version (20K):
[in this window]
[in a new window]
|
Figure 1.
Cell fate: instructed by parents or neighbors? A
schematic representation of possible mechanisms to specify cell
identity. White, Unspecified cell. Gray, Specified cell. Ellipse,
Information for specification. A, Lineage-based mechanism for
specification. B, Position-based mechanism for cell specification. C,
Successive utilization of lineage- and position-based
mechanisms.
|
|
| |
PLANT PATTERNING IN THE 1970s |
An important role for cell lineage in the acquisition of cell
identity was derived more than a century ago from the regular layering
of cells in shoot and root apices (8). Later studies stressed
variability in cell division patterns (4) and flexibility of plant cell
fate in meristems and tissue culture (1, 21, 17). Textbooks on plant
development that appeared in the early 1970s used this information to
reject lineage-based scenarios for shoot development, but a more
pronounced role for lineage in root meristems was still considered
possible (5, 19). The textbooks of the 1970s provided essentially two
different explanations for position-dependent cell differentiation. On
the one hand, nutrients and growth factors were supposed to form a
network of stimuli for cell differentiation, and from tissue culture
experiments it was extrapolated that pattern formation was under the
control of balances between phytohormones (5). On the other hand, Jacob
and Monod's lac operon model inspired the notion that
shifting patterns of gene expression could accomplish cell
differentiation (19).
Physiological control and gene regulation were mentioned in the 1977 and 1978 editions of widely read plant anatomy books of Esau and
Cutter. Thus the plant community of the 1970s widely appreciated the idea that pattern formation resulted from
position-dependent interactions with little emphasis on cell lineage.
| |
MOSAIC ANALYSIS CONFIRMED THE IMPORTANCE OF POSITIONAL
INFORMATION |
Periclinal chimeras
genetically different ("mosaic") cell
clones with an easily scorable phenotypic trait (e.g. albinism or ploidy level)were already known for decades and were shown to span
one of the parallel layers of a shoot apical meristem (11). For a
considerable period of time, chimeras were studied mainly to determine
how many stem cells ("initials") existed in each layer of the shoot
apical meristem. A new and very important realization occurred in the
early 1970s, but was not yet emphasized in prominent textbooks: rare
cell layer invasion events, observed in chimeras, provided strong
evidence that stem and leaf cell fate was determined by position rather
than by lineage even at late stages of development (20). The
realization that mosaic sectors could provide detailed information on
cell fate restriction was subsequently taken up, and refined versions
of mosaic analysis in the 1970s and 1980s provided us with a detailed
view on the flexible ontogeny of cellular patterns in many plants (10).
| |
GENES FOR PATTERN FORMATION, TRANSCRIPTION FACTORS FOR
IDENTITY |
Landmark papers on mutational analysis of pattern formation in the
fruit fly changed the entire field of developmental biology around
1980. Systematic analysis of developmental mutants and isolation of the
corresponding genes allowed investigators to describe development in
terms of the ordered activity of gene products in space and in time. In
the mid-1980s, the identification of many of these genes led to the
isolation of instructive molecules that directed the expression of
transcription factors (TFs) to groups of cells in the fruit fly (15, 18). These TFs, often of the homeodomain class, then instructed cell
identity. Whereas positional signaling was important to dictate the
expression of specific TFs in cells at early stages, their stable
transcription was later ensured by cell-autonomous mechanisms (encoded
among others by "Polycomb Group" genes). The responsible gene
products allowed the stable inheritance of a TF expression profile by
progeny cells and hence provided nuts and bolts for a lineage-based
mechanism of fate propagation. A description of the reproducible cell
lineage of the soil nematode Caenorhabditis elegans
gave new support to the idea that lineage strategies might dominate in
some multicellular organisms. However, subsequent molecular genetic
analyses clarified that much of this lineage invariance reflected the
reproducible outcome of positional signaling mechanisms (3). Thus it
was convincingly shown that reproducible lineage in the worm did not
automatically imply lineage-based mechanisms. On the other hand, early
position-dependent activation of TFs was fixed in some worm cell
lineages, and these changes modified the response of cells to
later-acting positional cues (hence, making late positional signaling
responses "lineage-dependent").
In summary, molecular-genetic dissection of fly and worm development
revealed an alternation of lineage- and position-dependent mechanisms
for the specification of cell fate (Fig. 1C).
| |
MOLECULAR GENETICS IN PLANT DEVELOPMENT |
Undoubtedly inspired by the new successes in animal development,
molecular genetic analysis of plant development took off in the
mid-1980s. The maize KNOTTED gene was shown to encode a homeodomain protein with similarity to animal TF-encoding lineage selector genes, and genes encoding TFs of the MADS-box class formed a
combinatorial code to specify cell fates in floral primordia of
Arabidopsis (2, 7). These findings marked a change in perception that
pervaded the plant sciences, as they emphasized the establishment of
distinct cell lineages by TFs. In a similar vein, genetic dissection of
embryogenesis in Arabidopsis resulted in mutants that were at first
interpreted to signify the early establishment of distinct embryonic
lineages. Soon thereafter, detailed analysis of these embryo-defective
mutants and clonal analysis of embryogenesis led to the abandonment of
this lineage-centered view on embryogenesis and renewed emphasis was
put on positional information in combination with lineage-propagated
differences in responsiveness to these cues (9). Manipulation of cell
position by laser ablation and other experiments demonstrated that even
in the Arabidopsis root, with the type of cell lineage regularity that
led to the proposition of lineage-based mechanisms more then a century
ago, cell-to-cell signaling was of crucial importance for the
acquisition of cell identity (12). So, halfway into the 1990s, an
important role for positional information in cellular patterning of
plants surfaced again.
| |
IDENTIFYING MECHANISMS OF PLANT CELL PATTERNING |
A tremendous accumulation of genetic and molecular data over the
last 5 years has begun to provide the first glimpses of pattern formation mechanisms. Three examples relevant for this discussion will
be given below.
First, it was discovered that a Polycomb group-like gene controlled
late repression of AGAMOUS (AG), one of the MADS-box TFs involved in
floral organ identity (6). This finding, together with earlier
observations on temperature-sensitive apetala2
(ap2) alleles, suggested that restriction of AG by spatial
regulation through other TFs (like AP2) was only required early in
flower development, and that MADS-box protein expression might be
controlled by a lineage-mechanism of cell fate at later stages of
development. The recent successful generation of Cre-loxP
based ag
clones (16) should now allow us
to distinguish between spatial or lineage-based regulation at late
stages of flower development.
Second, insight into the specification of cell types has come from
molecular-genetic analysis of trichome formation. Evidence is
accumulating that transcription factors like GLABRA1, required for the
determination of trichome cell fate, may initiate (by influencing the
production of inhibitors of their own activity that act in neighboring
cells) and be the target of cell-to-cell communication involved in
pattern formation, creating self-regulatory loops (13). In this case of
pattern formation, cells decide on their fate only after the last cell
division, and hence do not transmit this decision to their progeny
through lineage-based mechanisms.
Third, a network of interacting gene products consisting of homeodomain
transcription factors (such as WUSCHEL) and transmembrane signaling
components (such as the CLAVATA1-3 proteins) appears to regulate the
size of the stem cell population of the shoot apical meristem and of
subjacent organizing cells. The current view is that cell-to-cell
signaling from CLV3-expressing stem cells regulates the pool size of
WUSCHEL-expressing cells and vice versa (14). Thus a homeodomain
transcription factor that is required for the identity of a group of
cells remains subject to continuous regulatory input from neighboring
cells, and hence is not maintained by cell-autonomous mechanisms.
Similar cell-to-cell signaling events might operate over long periods
of time to maintain cell fate differences in other plant regions.
| |
CONCLUSIONS |
Twenty-five years ago, a major role for positional information in
plant cell fate specification was generally accepted. Clonal analyses
in the 1970s and 1980s reinforced concepts of position-dependent differentiation that were hitherto mostly derived from intrusive surgical approaches. However, it took molecular genetic approaches to
begin the dissection of mechanisms of cell specification. As in
animals, lineage- and position-based mechanisms operating in succession
are tentatively identified in plants, although many components
are still missing. At this stage it is premature to assess how
frequently either of these mechanisms is used and how they interact.
Nevertheless, it seems plausible that position-dependent mechanisms
operate all the time in embryos and indeterminate meristems and that
lineage mechanisms to pass cell fate decisions on to progeny may act in
more limited time windows. Such a ratio of relative importance would
account for much of the prolonged flexibility that is seen in plant development.
| |
ACKNOWLEDGMENTS |
I apologize for the fact that only a few relevant research
contributions could be cited due to severe space limitations. I would
like to thank Ian Sussex and the members of my laboratory for critical
reading of the manuscript.
| |
FOOTNOTES |
*
E-mail b.scheres{at}bio.uu.nl; fax 31-30-2513655.
| |
LITERATURE CITED |
-
Ball E
(1952)
Growth
16: 91-110
-
Coen ES, Meyerowitz EM
(1991)
Nature
353: 31-37
[CrossRef][Medline]
-
Emmons SW
(1987)
Cell
51: 881-883
[CrossRef][Web of Science][Medline]
-
Foster AS
(1939)
Bot Rev
5: 454-470
-
Galston AW, Davies PJ
(1970)
Control Mechanisms in Plant Development. Prentice-Hall, New Jersey
-
Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G
(1997)
Nature
386: 44-51
[CrossRef][Medline]
-
Hake S
(1992)
Trends Genet
8: 109-114
[Medline]
-
Hanstein J (1868) Festschr Niederrhein Ges Natur
u Heilk 109-143
-
Jürgens G
(1995)
Cell
81: 467-470
[CrossRef][Web of Science][Medline]
-
Poethig RS
(1987)
Am J Bot
74: 581-594
[CrossRef][Web of Science]
-
Satina S, Blakesly AF, Avery AG
(1940)
Am J Bot
27: 895-905
[CrossRef][Web of Science]
-
Scheres B
(1997)
Curr Opin Genet Dev
7: 501-506
[Medline]
-
Schnittger A, Folkers U, Schwab B, Jürgens G, Hülskamp M
(1999)
Plant Cell
11: 1105-1116
[Abstract/Free Full Text]
-
Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T
(2000)
Cell
100: 635-644
[CrossRef][Web of Science][Medline]
-
Scott MP, Carrol SB
(1987)
Cell
51: 689-698
[CrossRef][Web of Science][Medline]
-
Sieburth LE, Drews GN, Meyerowitz EM
(1998)
Development
125: 4303-4312
[Abstract]
-
Skoog F, Miller CO
(1957)
Symp Soc Exp Biol
11: 118-131
-
St. Johnston D, Nüsslein-Volhard C
(1992)
Cell
68: 201-219
[CrossRef][Web of Science][Medline]
-
Steeves TA, Sussex IM
(1972)
Patterns in Plant Development. Prentice-Hall, New Jersey
-
Stewart RN, Burk LG
(1970)
Am J Bot
57: 1010-1016
[CrossRef][Web of Science]
-
Sussex IM
(1952)
Nature
170: 224-225
© 2001 American Society of Plant Physiologists
TOP
INTRODUCTION
PLANT PATTERNING IN THE...
