Nanospherical arabinogalactan proteins are a key component of the high-strength adhesive secreted by English ivy

Abstract

Over 130 y have passed since Charles Darwin first discovered that the adventitious roots of English ivy (Hedera helix) exude a yellowish mucilage that promotes the capacity of this plant to climb vertical surfaces. Unfortunately, little progress has been made in elucidating the adhesion mechanisms underlying this high-strength adhesive. In the previous studies, spherical nanoparticles were observed in the viscous exudate. Here we show that these nanoparticles are predominantly composed of arabinogalactan proteins (AGPs), a superfamily of hydroxyproline-rich glycoproteins present in the extracellular spaces of plant cells. The spheroidal shape of the AGP-rich ivy nanoparticles results in a low viscosity of the ivy adhesive, and thus a favorable wetting behavior on the surface of substrates. Meanwhile, calciumdriven electrostatic interactions among carboxyl groups of the AGPs and the pectic acids give rise to the cross-linking of the exuded adhesive substances, favor subsequent curing (hardening) via formation of an adhesive film, and eventually promote the generation of mechanical interlocking between the adventitious roots of English ivy and the surface of substrates. Inspired by these molecular events, a reconstructed ivy-mimetic adhesive composite was developed by integrating purified AGP-rich ivy nanoparticles with pectic polysaccharides and calcium ions. Information gained from the subsequent tensile tests, in turn, substantiated the proposed adhesion mechanisms underlying the ivy-derived adhesive. Given that AGPs and pectic polysaccharides are also observed in bioadhesives exuded by other climbing plants, the adhesion mechanisms revealed by English ivy may forward the progress toward understanding the general principles underlying diverse botanic adhesives.ivy nanoparticle | ivy adhesive | arabinogalactan protein | adhesion mechanism | reconstructed adhesive A lthough there is a growing interest in exploring mechanisms regulating a variety of adhesive behaviors in the animal kingdom (1-6), the molecular basis allowing creeping plants, such as English ivy (Hedera helix), to generate sufficient adhesive force, aiding in clinging to vertical surfaces, is rarely discussed (Fig. 1A). Previous studies have emphasized mechanical strategies exploited by multiple climbing organs that evolve in plants (7-11). Nevertheless, the role of the glue-like viscous exudates that are observed on the majority of these organs and that cement the plants to the substrates has been less explored (10,12,13). Diverse polysaccharides and glycoproteins, comprising mucilaginous pectins, arabinogalactans, arabinogalactan proteins (AGPs), and many others, have been identified to be the predominant components in these adhesive substances (14-17); however, the molecular mechanisms underlying the high-strength adhesion remain elusive.By means of atomic force microscopy (AFM), bulk spherical organic nanoparticles have been observed in the exudates derived from the root hairs of English ivy (18-20). These proteinaceous nanoparticles are presum...

Sticky mucilages and exudates of plants: putative microenvironmental design elements with biotechnological value

“…A study of the attachment organs of climbing fig (Ficus pumila) and English ivy (Hedera helix) identified clusters of adventitious roots as the organ from which an adhesive mucilage that robustly secures the plant to vertical surfaces is secreted (Groot et al, 2003;Melzer et al, 2010). A detailed compositional analysis has been so far only performed for H. helix (Huang et al, 2016) and revealed that the major components of the mucilage secreted by English ivy are pectic rhamnogalacturonan-I (RG-I) polysaccharide domains that are held together by a nanospherical arabinogalactan protein (AGP) molecule (Table 1). A detailed compositional analysis has been so far only performed for H. helix (Huang et al, 2016) and revealed that the major components of the mucilage secreted by English ivy are pectic rhamnogalacturonan-I (RG-I) polysaccharide domains that are held together by a nanospherical arabinogalactan protein (AGP) molecule (Table 1).…”

“…Virginia creeper (Parhenocissus quinquefolia), by contrast, produces adhesive discs at the end of short tendrils for climbing (Bowling & Vaughn, 2008). This multipolysaccharide architecture is supported by calcium-driven electrostatic interactions between the acidic residues of the AGP and RG-I domain (Huang et al, 2016). This multipolysaccharide architecture is supported by calcium-driven electrostatic interactions between the acidic residues of the AGP and RG-I domain (Huang et al, 2016).…”

“…A very promising approach that has yielded major breakthroughs in recent years is the use of techniques enabling visualisation of nanostructures (Huang et al, 2015(Huang et al, , 2016. Some molecules present in these mucilages possess naturally adhesive properties that have potential biotechnological and biomedical value in the form of glues or wound coversalthough the precise bioadhesive molecules present in the secretions have rarely been identified.…”

“…Being sessile and unable to evade unfavourable conditions, their survival depends critically on their ability to sense their environment and, if possible, create favourable local conditions. Classic examples include the capacity of climbing plants to climb up vertical surfaces using sticky tendrils or roots (Endress & Thomson, 1977;Groot et al, 2003;Huang et al, 2016). Plants have also evolved ways to bioengineer favourable microenvironments in their immediate surroundings by the secretion or exudation of mucilages from various surfaces.…”

“…Mucilages and other exudates provide an effective means to execute a variety of functions beyond the confines of their tissues and organ surfaces. Classic examples include the capacity of climbing plants to climb up vertical surfaces using sticky tendrils or roots (Endress & Thomson, 1977;Groot et al, 2003;Huang et al, 2016). Other types of exudates are produced by leaves or by stems and have become known as extrafloral nectars (Deynze et al, 2018;Pierce, 2019).…”