Development on the rocks: Integrating molecular biology and the fossil record to reconstruct the evolution of leaf development

Leaves, encountered in the majority of modern tracheophytes, evolved multiple times independently in several lineages. We define leaves as lateral appendages that share a common set of characters: vascularization, determinacy, regular arrangement, bilateral symmetry and, in most cases, adaxial-abaxial (dorsiventral) polarity. In this review we integrate data from developmental genetics and the fossil record to understand how the molecular and cellular mechanisms of leaf development evolved. We show that lycopsid leaves likely evolved once, and earlier, than euphyllophyte leaves, and that euphyllophyte leaves all evolved from lateral branching systems that were produced at regular intervals around the stem. We also show that the mosaic pattern of distribution and tempo of evolution of leaf-defining features (such as bilateral symmetry and dorsiventral polarity) among the different lineages suggests that these features evolved independently. Overall, at the level of the entire tracheophyte clade, integration of developmental, regulatory and fossil data reveals three overarching patterns: (1) the different leaf characters evolved independently throughout tracheophyte phylogeny and their regulatory pathways were assembled independently, only to become tightly integrated with each other later in the evolution of different lineages; (2) bilateral symmetry is a distinct and evolutionarily independent leaf feature from dorsiventral polarity; (3) regular arrangement is the most plesiomorphic and earliest-evolving leaf-defining feature across tracheophytes.