Developmental programmes in the evolution of Equisetum reproductive morphology: a hierarchical modularity hypothesis.

Background: The origin of the Equisetum strobilus has long been debated and the fossil record has played an important role in these discussions. The paradigm underlying these debates has been the perspective of the shoot as node-internode alternation, with sporangiophores attached at nodes. However, fossils historically excluded from these discussions (e.g. Cruciaetheca and Peltotheca ) exhibit reproductive morphologies that suggest attachment of sporangiophores along internodes, challenging traditional views. This has rekindled discussions around the evolution of the Equisetum strobilus, but lack of mechanistic explanations has led discussions to a stalemate. Scope: A shift of focus from the node-internode view to a perspective emphasizing the phytomer as a modular unit of the shoot, frees the debate of homology constraints on the nature of the sporangiophore and inspires a mechanism-based hypothesis for the evolution of the strobilus. The hypothesis, drawing on data from developmental anatomy, regulatory mechanisms and the fossil record, rests on two tenets: (1) the equisetalean shoot grows by combined activity of the apical meristem, laying down the phytomer pattern, and intercalary meristems responsible for internode elongation; and (2) activation of reproductive growth programmes in the intercalary meristem produces sporangiophore whorls along internodes. Conclusions: Hierarchical expression of regulatory modules responsible for (1) transition to reproductive growth; (2) determinacy of apical growth; and (3) node-internode differentiation within phytomers, can explain reproductive morphologies illustrated by Cruciaetheca (module 1 only), Peltotheca (modules 1 and 2) and Equisetum (all three modules). This model has implications - testable by studies of the fossil record, phylogeny and development - for directionality in the evolution of reproductive morphology ( Cruciaetheca - Peltotheca - Equisetum ) and for the homology of the Equisetum stobilus. Furthermore, this model implies that sporangiophore development is independent of node-internode identity, suggesting that the sporangiophore represents the expression of an ancestral euphyllophyte developmental module that pre-dates the evolution of leaves.