Evo-Devo of Leaves: A Story Told by Ferns and Lycophytes

Biologists have been intrigued by the origin of novelties for centuries. Leaves are novel plant organs and can serve as an excellent model for understanding the origin and evolution of novelties. Morphological, paleobotanical, and phylogenetic analyses have failed to concur on the origin of leaves or even how many times leaves have evolved in vascular plants. In addition, previous comparative expression analyses in lycophytes and seed plants have come to diametrically opposed conclusions about the conservation of a leaf developmental program. We conducted phylogenetic analyses of leaf developmental gene families (Class III HD-Zip, KNOX, CUC) across land plants with extensive new data across lycophytes and ferns. We also utilized comparative expression analyses of orthologous genes by in situ hybridization. We performed our expression analyses in both vegetative and reproductive organs of lycophytes and ferns. Here, we provide the first molecular genetic support indicating a conservation in a leaf developmental program between ferns and seed plants. In addition, our results show Class III HD-Zip expression in sporangia (reproductive organs) across lycophytes and ferns. This provides the first molecular genetic evidence that a sporangia developmental network was co-opted independently for the evolution of all leaves. Furthermore this shifts the paradigm of lycophyte leaf evolution from the widely cited enation theory to the sterilization of sporangia theory.