Comparison of animal and plant development: a right track to establish a theory of development?

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1 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 vervoort.michel@ijm.univ-paris-diderot.fr

2 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).

3 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.

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5 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.

6 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.

7 This reasoning however faces one major obstacle which is homology.

8 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.

9 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,

10 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.

11 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

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13 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

14 Possible pitfalls and obstacles in the use of the comparison of animal and plant development to build a theory of development

15 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

16 Comparisons between animal and plant development: a case study - the specification of body parts and tissue identities Hox and floral identity genes - homeotic genes

17 Hox genes

18 Floral identity genes

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21 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.

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23 This very sophisticated regulation of the activity of Hox and floral identity genes illustrates two important features of their role during body part specification.

24 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.

25 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.

26 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.