© 1987 by The Society for Integrative and Comparative Biology
Inheritance of Pattern: Analysis from Phenotype to Gene1
Department of Biological Sciences, Stanford University Stanford, California 94305
The form and pattern of multicellular organisms are developmental phenotypes. They are long term processes rather than static structures. They involve myriad events at multiple locations. The efficient encoding of such phenotypes is analyzed here in two stages. First, the complex developmental behavior is broken down so it can be accounted for by cell or tissue rules. The most effective rules have the instantaneous character found in time-based differential equations. When integrated over time and space, the rules produce the behavior. Second, the cytological and nuclear basis of the rules is sought. One thus studies a complex phenotype in terms of its successive antecedent causes, refining understanding as one gets closer to the genome.
The approach is applied here to phyllotactic (leaf placement) patterns. Leaves may be alternating in a plane, whorled, or in a helical arrangement. In all three cases a new leaf forms as an arc-like bulge at a site apical to a small number of neighboring leaves. The leaf-forming sites are irregularities in the pattern of cellulose reinforcement in the surface of the apical dome. Two organ-level rules combine to produce new leaf sites. First, each established leaf develops a single reinforcement field, with gently curved reinforcement lines, on the region of the dome just above the leaf. Second, where parts of two or three such fields abut on the dome they combine to make the irregularity for the next leaf. Hence a given reinforcement pattern on the dome produces a leaf; the action of the leaves in turn reestablishes the reinforcement pattern. The cellular basis of generating a reinforcement field appears to be a cytoskeletal response to excessive stretch, brought on by rapid growth of adjacent leaf bases. The large scale patterns are thus traceable to cytoskeletal phenomena and from there to genes involving microtubular behavior.