A Passionate Free Climber: Structural Development and Functional Morphology of the Adhesive Tendrils in Passiflora discophora

Abstract

Editor: Adrienne NicotraPremise of research. Passiflora discophora is exceptional among passion flowers for its climbing strategy, using branched tendrils with terminal adhesive pads instead of coiling tendrils as typical within this family. This article investigates the structural development and morphology of these adhesive pads and aims to understand the underlying structure-function relationship of the attachment process. Based on our results, we discuss possible mechanical consequences of the tendril structure and compare our findings with similar attachment systems in unrelated species in order to identify general strategies of this mode of attachment.Methodology. We investigated the temporal development of the attachment process, including detailed studies of the morphology and anatomy of the adhesive pads, using LM with different staining procedures and SEM.Pivotal results. Young tendrils establish initial contact with a supporting substrate by interlocking with their hook-shaped tips. Touch stimuli induce the tips to develop into adhesive pads by callus-like growth of papillate epidermal cells. Fully grown pads are hemispherical on flat substrates or completely fill out larger cavities of the substrate. By apical cell division, the pad tissue perfectly mimics the microtopography of the substrate and also grows into minute gaps and fissures, establishing firm anchorage by optimal form closure. Additionally, an extracellular substance is visible at the interface between pad and substrate surface, which might act as adhesive.Conclusions. The opportunistic growth and cellular structure make the tendrils and adhesive pads of P. discophora a highly adaptive attachment system. Comparison with other not closely related taxa reveals general principles of this climbing mode, namely, (1) branched tendrils with multiple adhesive pads, (2) papillate cells establishing optimal form closure with the substrate and in some species additionally secreting adhesive substances, (3) free coiling of axes, and (4) persisting anchorage after senescence.

Convergent Evolution and the Diverse Ontogenetic Origins of Tendrils in Angiosperms

“…Nevertheless, some species from the subgenus Deidamioides show branched tendrils with terminal adhesive pads, a feature that is exclusive to this subgenus (Krosnick et al, 2013 ). This is the case in three species of Passiflora , i.e., Passiflora discophora, P. arbelaezii , and P. tryphostematoides (Bohn et al, 2015 ). Tendrils of P. discophora are 3-to-5 branched with terminal adhesive pads.…”

“…Tendrils of P. discophora are 3-to-5 branched with terminal adhesive pads. A recent developmental analysis of P. discophora revealed that tendrils perform contact coiling that is combined with the development of adhesive pads for climbing (Bohn et al, 2015 ). Before initial contact with a substrate, tendril apices are slightly hook shaped.…”

“…The proliferation of papillate cells leads to the formation of the pad, with a porous surface. This porous pad tissue develops at the tendril tips and along portions of the tendril axes that are in contact with the substrate (Bohn et al, 2015 ). Differently from Parthenocissus , the pads of P. discophora tendrils adapt to the topography of the substrate, and thus have varied shapes; when growing on flat supports they have a hemispherical shape.…”

“…Differently from Parthenocissus , the pads of P. discophora tendrils adapt to the topography of the substrate, and thus have varied shapes; when growing on flat supports they have a hemispherical shape. P. discophora also produces an adhesive fluid, that is made of cutin and lipids, and mainly concentrated in the central part of the contact zone (Bohn et al, 2015 ). The fluid enhances the form closure by filling micro- and nanogaps and intercellular spaces in the contact zone (Bohn et al, 2015 ).…”

Rose Prickles and Asparagus Spines – Different Hook Structures as Attachment Devices in Climbing Plants

“…In this respect the hook structures of semi-self-supporting plants differ fundamentally from attachment devices of climbing plants which establish a much closer attachment to the host plants which is necessary as these climbers entirely have lost mechanical (self-)stability of their stems in older ontogenetic stages. Coiling tendrils, adventitious roots with root hairs or adhesive pads secure a much closer attachment to the host plants and adhere much firmer to their supporting structures [ 1 , 18 – 22 ]. In these plants typically flexible structures (e.g.…”