Oral Paper

         Paleobotany

Probing the origin and evolution of periderm: what can extant plants and the fossil record tell us?

Presenting Author
Madison Lalica
Description
Secondary growth arises from the activity of lateral meristems - the vascular cambium and the cork cambium. The latter, and the tissues it produces, are collectively referred to as periderm. Periderm occurs as a typical ontogenetic phase forming protective outer tissues (canonical or native periderm), or in association with abscission areas, or as a self repair process that seals wounds (wound periderm). We review wound periderm in the broader context of periderm-type secondary growth and update the scarce data on occurrences of wound periderm outside the spermatophyte clade. In extant plants, periderm (wound and canonical) has been documented and studied extensively in spermatophytes but is exceedingly rare among the seed-free plants. The rarity of canonical periderm among the latter is nevertheless belied by occurrences of wound periderm across a broader taxonomic range of seed-free plants. Sparse published records and our own wounding experiments demonstrate that wound periderm is produced by ophioglossalean, marattialean, and filicalean ferns. In the fossil record, canonical periderm was documented in several seed-free lineages - isoetalean lycophytes, cladoxylopsids, sphenopsids, progymnosperms. Its oldest documented occurrence (Middle Devonian; Givetian) is pre-dated by that of wound periderm in the Early Devonian, 15 million years prior. This suggests that periderm evolved as a wound response mechanism that was subsequently co-opted in canonical developmental pathways to seal off outer tissues that were put under tensional stress due to significant vascular cambial growth; and that wound periderm is a conserved feature, whereas canonical periderm may have been gained and lost throughout evolutionary history. Along with its murky origins, an incompletely explored aspect of periderm regards developmental mechanisms as related to canonical vs wound periderm in seed-free vs seed plants. Namely while some periderms show consistent organization - regular layering, a well-defined cambial layer, and clear bifacial polarity (cork/phelloderm) - others are less organized, lacking consistent layering as well as a conspicuous cambial layer and bifacial polarity. Therefore, what has been considered as a single type of tissue and referred to as periderm may include two distinct types of tissue significantly different in their development and anatomy. While both types develop by periclinal divisions, in one type these divisions are spatially coordinated (organized periclinal growth), whereas in the other type they occur concurrently at several depths in the tissue of origin (diffuse periclinal growth). A preliminary survey suggests that wound periderm develops exclusively by diffuse periclinal growth outside the seed plants, whereas in seed plants it may form mostly by organized periclinal growth. Because the oldest wound periderms of the Early Devonian were produced by diffuse periclinal growth, it is possible that this periderm development mode preceded and gave rise to organized periclinal growth. Testing these hypotheses about periderm evolution will require broadening the taxonomic scope of wounding experiments in seed-free plants, in parallel with application of methods (histological staining, UV autofluorescence) to characterize the organization and assess developmental bifaciality in wound and canonical periderm in both seed-free plants and spermatophytes, and will benefit from additional discoveries of periderm in the Devonian fossil record.