Modularity and hierarchy: development meets the fossil record in a hypothesis for the origin of the Equisetum strobilus.

TOMESCU, ALEXANDRU M. F.; ESCAPA, IGNACIO; ROTHWELL, GAR

Savannah

Congreso; Botany 2016; 2016

Botanical Society of America

The origin and homologies of the Equisetum strobilus and sporangiophore have been debated for well over a century. The prevailing paradigm underlying these debates has been the traditional perspective that views the shoot as an alternation of nodes and internodes. In this perspective, sporangiophores are regarded as appendages attached at nodes and the fossil record has been called upon to assemble transformational series explaining the evolution of the sporangiophore and strobilus. However, a number of fossil sphenopsids historically excluded from these discussions exhibit reproductive morphologies that suggest attachment of sporangiophores along internodes, challenging the traditional view of the sporangiophore as appendage attached at a node. Such morphologies, illustrated by Cruciaetheca and Peltotheca, have rekindled debates on the evolution of the Equisetum strobilus, but a lack of mechanistic explanations has led these discussions to a stalemate. To circumvent this impasse, we propose a shift of focus from the traditional node-internode view to another traditional perspective that emphasizes the phytomer as the modular growth unit of the shoot. This perspective frees the debate of constraints associated with homology assumptions on the nature of the sporangiophore. It also inspires a mechanism-based hypothesis for the evolution of the strobilus. This new hypothesis is supported by data from developmental anatomy, growth regulation mechanisms, teratological forms, and from the fossil record. It rests on two tenets: (i) growth of the equisetalean shoot arises from the combined activity of the apical meristem, which lays down the phytomer pattern, and intercalary meristems responsible for internode elongation within each phytomer; and (ii) plant meristems are equicompetent and shared genetic switches can turn on reproductive growth programs in the intercalary meristem where they lead to production of sporangiophore whorls with a basipetal maturation pattern. Within this framework, hierarchical expression of three regulatory modules responsible for (1) the (reversible) transition to reproductive growth, (2) determinacy of apical growth, and (3) node-internode differentiation within phytomers, produces the reproductive morphologies illustrated by Cruciaetheca (module 1 only), Peltotheca (modules 1 and 2), and Equisetum (all three modules). This nested set of hypotheses has implications, which are 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.