Download Comparison of animal and plant development: a right track to

Comparison of animal and plant
development: a right track to
establish a theory of development?
Michel Vervoort
Institut Jacques Monod
CNRS / Université Paris Diderot -Paris 7
e-mail: [email protected]
Development comprises a set of operations that allow
the transition from single cells to complex multicellular
assemblies. This includes coordinated cell proliferation,
setting up of polarities (such as anterior-posterior
polarity in animals), cell differentiation, establishment of
shapes (morphogenesis) and patterns of cell
differentiation (e.g. Bonner 2000).
There could be principles that underly these
developmental operations and that would be valid for
all organisms displaying a development. These
principles would therefore be independent of the
evolutionary position and history of the organisms. In
other words, this means that there could be ways to
proceed that should be followed during development,
irrespective of whether the developing organism is an
animal, a plant, or any other multicellular organism.
What I propose is to identify principles that together would
constitute an ‘anhistorical theory of development’ that
focuses on what unifies all types of development.
How to build such a theory?
A comparative approach is required: one can reasonably argue
that ‘principles of development’ will be related to observations
that have been made in more than one species, ideally in many
or all the studied species. On the contrary, mechanisms or
processes that are specific to a single species and/or a single
developmental event are unlikely to be considered as general
developmental principles.
This reasoning however faces one major
obstacle which is homology.
This reasoning however faces one major
obstacle which is homology.
Indeed, in case of homology, the repeated observation in
different species of similar mechanisms or processes may
therefore not point out the type of principles of development
that I propose to define, but simply reflects the inheritance
of developmental processes or mechanisms by the presentday species from their last common ancestor.
This reasoning however faces one major
obstacle which is homology.
Indeed, in case of homology, the repeated observation in
different species of similar mechanisms or processes may
therefore not point out the type of principles of development
that I propose to define, but simply reflects the inheritance
of developmental processes or mechanisms by the presentday species from their last common ancestor.
I argue that only the comparison of convergent
developmental processes can be useful to
establish a ‘nonhistorical’ theory of development,
I suggest to focus on processes for which we have compelling
evidence for the absence of homologies in the underlying
mechanisms. A way to do so is to compare the development of
multicellular organisms that belong to distantly-related
eucaryotes, in particular plants and animals.
Development of animals and plants largely relies on convergent
processes - Phylogenetic evidence: the last common ancestor
of plants and animals was likely an unicellular organism
Development of animals and plants largely relies on
convergent processes - Molecular evidence: developmental
processes in plants and animals show some similarities, but
mostly rely on non-homologous molecules
Possible pitfalls and obstacles in the use of the comparison of
animal and plant development to build a theory of development
Possible pitfalls and obstacles in the use of the comparison of
animal and plant development to build a theory of development
1. The first one is the paucity of such comparisons in the
existing literature
2. A second and very serious pitfall is that the comparisons
may lead to useless truisms rather than useful principles
3. A third possible obstacle is the representativeness of the
species from which the data to be compared have been
acquired
4. A fourth possible problem would be that the observed
similarities between plant and animal development, although
the processes have been independently acquired, might
nevertheless be related to homologies - ‘deep homology’
Comparisons between animal and plant development: a case
study - the specification of body parts and tissue identities
Hox and floral identity genes - homeotic genes
Hox genes
Floral identity genes
We can therefore suggest that a principle of cell/tissue/organ/
body part specification is to rely on the function of ‘input-output
genes’ that make the link between various spatiotemporal
informations and the differentiation of specific structures.
A testable prediction of this suggestion is that ‘input-output
genes’ should be found in a large number of identity
specification events during the development of animals, plants,
and other eukaryotic multicellular organisms.
This very sophisticated regulation of the activity of Hox and
floral identity genes illustrates two important features of their
role during body part specification.
This very sophisticated regulation of the activity of Hox and floral identity genes
illustrates two important features of their role during body part specification.
First is the fact that in the case of selector genes, it
is equally important that these genes are expressed
and active in some cells and that they are not
expressed and/or active in other ones.
Several layers of negative regulation are thus
required and the comparison between plant and
animals homeotic genes suggests that crossinhibition, i.e. the activity of some selector genes
interfering with that of (an)other selector gene(s), and
regulation by miRNAs seem to be efficient ways to
achieve the required tight regulation of the
expression of selector genes.
This very sophisticated regulation of the activity of Hox and floral identity genes
illustrates two important features of their role during body part specification.
A second key feature is the need for sustained
expression of the selector genes during the whole
body part specification process.
Based on the comparison between animal and plant
homeotic genes, the combination of autoregulation
and epigenetic maintenance seems to be the
efficient way to achieve the sustained expression of
selector genes involved in body plan.
Conclusions
I developed the idea that a theory of development can be built
through the comparison between developmental processes in
animals and plants.
More specifically, this comparison would lead to define
common anhistorical properties of development in these two
lineages, as the convergent nature of their developmental
processes allows to exclude euhistorical properties due to
homology and common ancestry.
This would hopefully lay the groundwork for the identification of
general principles of development that would be valid for all
multicellular organisms.