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Dasycladales morphogenesis: the pattern formation viewpoint Dumais, Jacques


The Dasycladalian algae produce diverse whorled structures, among which the best-known are the reproductive whorl (cap) and the vegetative whorls (hair whorls) of Acetabularia acetabulum. The origin of these structures is addressed in terms of three pattern forming mechanisms proposed to explain whorl formation. The mechanisms involve either: mechanical buckling of the cell wall, reaction-diffusion of morphogens along the cell membrane, or Ca²⁺-cytoskeleton mechanochemical interactions in the cytosol. They are described and their idiosyncrasies underlined to provide a ground to test them experimentally. It is also suggested that the closely regulated spacing between the elements of a whorl is a key component of such a test. A detailed staging of whorl formation in the genus Acetabularia shows that the elements constituting the whorl can be traced back to their initiation as localized wall lysis. Stagings of the genera Polyphysa, Batophora, Halicoryne, and Neomeris are also provided. The succession of wall thickening and wall lysis as well as the spacing observed are to some extent incompatible with the idea of wall buckling. The stagings show also the homology between the reproductive and vegetative whorls. Of the different homological systems proposed, one is singled out based on a re-interpretation of the gametophore as a sui generis organ instead of its more common interpretation as a modified hair. Based on this evidence and that provided by the fossil record, it is shown that a reduction of the spacing within a whorl, the addition of one morphogenetic event for the gametophore and a redistribution of growth are sufficient to explain the major differences between the vegetative and reproductive whorls of several genera. More attention is given to the seemingly exceptional case of Halicoryne. A study of membrane-bound and free Ca²⁺ distribution during morphogenesis reveals that Ca²⁺ and growth are in lock step, yet there is no indication that Ca²⁺ would form a prepattern before morphological differentiation, thus providing some evidence that Ca²⁺ is not acting as a morphogen in a Ca²⁺-cytoskeleton morphogenetic mechanism. This discussion of morphogenesis in unicellular algae is shown to be relevant to higher plant morphogenesis given the deep similarities between tip growth and meristematic growth in terms of dynamics and models proposed. I conclude with suggestions for the study of pattern formation and for further research.

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