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Plant Cell Reports (2018) 37:565–574 https://doi.org/10.1007/s00299-017-2240-y

REVIEW

Climbing plants: attachment adaptations and bioinspired innovations

Jason N. Burris1 · Scott C. Lenaghan2,3 · C. Neal Stewart Jr.1

Received: 30 June 2017 / Accepted: 22 November 2017 / Published online: 29 November 2017 © Springer-Verlag GmbH Germany, part of Springer Nature 2017

AbstractClimbing plants have unique adaptations to enable them to compete for sunlight, for which they invest minimal resources for vertical growth. Indeed, their stems bear relatively little weight, as they traverse their host substrates skyward. Climbers possess high tensile strength and flexibility, which allows them to utilize natural and manmade structures for support and growth. The climbing strategies of plants have intrigued scientists for centuries, yet our understanding about biochemical adaptations and their molecular undergirding is still in the early stages of research. Nonetheless, recent discoveries are promising, not only from a basic knowledge perspective, but also for bioinspired product development. Several adaptations, including nanoparticle and adhesive production will be reviewed, as well as practical translation of these adaptations to commercial applications. We will review the botanical literature on the modes of adaptation to climb, as well as specialized organs—and cellular innovations. Finally, recent molecular and biochemical data will be reviewed to assess the future needs and new directions for potential practical products that may be bioinspired by climbing plants.

Keywords Nanoparticles · Tendrils · Hooks · Adhesion · Biomimicry · Engineering · Robotics

For centuries, scientists have been intrigued by the special-ized adaptations of climbing plants that enable them to com-pete for resources such as sunlight (Niklas 2011). Charles Darwin (1865) first categorized climbing plants based on their modes of attachment: twining, hook and leaf-bearers, tendril-bearers, and root climbers (Fig. 1). Thus, plants employ a diversity of strategies to use trees, bluffs, and now, human-created vertical structures to ‘cheat’ their way to sunlight. Their ability to cheat is a function of physical ‘engineering’ adaptations that are borne by largely unknown biochemical and biosynthesis mechanisms. Ecologically, climbers are renowned for optimizing resource acquisition while minimizing costs from metabolism (Gianoli et al. 2012).

Despite the prolonged fascination with climbing plants, we know surprisingly little about the molecular biology, genomics and biochemistry of attachment and climbing in plants. By way of contrast, we know much more about the mechanisms that certain animals employ to adhere to surfaces relative to that of climbing plants. For example, various animal systems have been extensively characterized, such as the attachment of marine invertebrates (e.g., Ben-edict and Picciano 1989; Lee et al. 2007; Lin et al. 2007; Sullan et al. 2009; Sangeetha et al. 2010) and the reversible adhesion systems of multiple species of arthropods, reptiles and amphibians (e.g., Artz et al. 2003; Huber et al. 2007; Kesel et al. 2003, 2004; Autumn 2006). With the rise in nanotechnology research, plants appear to be falling even farther behind animals with regards to analyzing their attach-ment systems.

Humans have a long history of ‘inventing-by-observation’ or copying innovations inspired by nature. Certainly, bioin-spired engineering continues to gain footholds in the era of systems and synthetic biology. Recent successes include the translation of the fundamental principles of animal attach-ment and climbing to robotics and adhesion (e.g., Awada et al. 2015; Kalouche et al. 2014; Palmer et al. 2009; San-tos et all. 2008; Seo et al. 2015; Gillies et al. 2013). We should now take further advantage of the world of climbing

Communicated by Chun-Hai Dong.

* C. Neal Stewart Jr. nealstewart@utk.edu

1 Department of Plant Sciences, University of Tennessee, 2431 Joe Johnson Dr., Knoxville, TN 37996-4561, USA

2 Department of Food Science, University of Tennessee, Knoxville, TN 37996, USA

3 Department of Mechanical, Aerospace, and Biomedical Engineering, University of Tennessee, Knoxville, TN 37996, USA

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plants for their adhesive properties, materials, and other innovations.

In this paper, we will briefly review the modes of climb-ing as classified by botanists. These modes will note specific examples of plants to illustrate the diversity of climbing. Second, we will explore what is known about molecular and biochemical mechanisms of climbing, with a focus on the adhesives and nanoparticles. Finally, we will propose new research directions as well as potential strategies to develop bioinspired products.

Evolution and taxonomic distribution of climbing plants

The ability to climb represents a diversity of biological inno-vations to acquire physical space, nutrients, and especially light, with minimal investment of resources by the climbing plant (Rowe et al. 2004; Paul and Yavitt 2011; Biernaskie 2011; Gianolli 2004, 2015a). Certainly, the resource-effi-cient strategies used among species are divergent and can be

illustrated by two examples of how climbers uniquely cope with biotic and abiotic stress. The first example is Convol-vulus chilensis Pers. (Convolvulaceae) (correhuela), which has evolved an elegant strategy in plant defense by climbing onto cacti and thorny shrubs as a defense from mamma-lian grazers (Atala and Gianoli 2008; Gonzales-Teuber and; Gianoli 2008). A second example is Ipomoea purpurea L. (Roth) (Convolvulaceae) (common morning glory), which induces twining as an apparent response to snail herbivory and drought conditions (Atala et al. 2014).

Taxonomically, vines (Vitaceae) are the most diverse climbers. When surveying 45 families of flowering plants, 38 taxa of climbers had higher diversity compared with their non-climbing sister groups, which suggests that climb-ing was a key innovation to niche utilization, competition (Schweitzer and Larson 1999), and diversification (Gianoli 2004). Additionally, one kingdom-wide survey found that 171 plant families contain at least one climbing plant spe-cies. They included nine fern families, two gymnosperm families, and families from three basal angiosperms, eight magnoliids, 22 monocots and 127 eudicots (Gianoli 2015b).

Fig. 1 Species illustrating some of Darwin’s (1865) modes of climb-ing. a Twiner Humulus lupulus, b hook climber Uncaria ovalifolia, c, leaf-bearer Galium aparine, d tendril-bearer Bryonia dioica. These examples denote the wide range of adaptations of climbing among angiosperms. All the illustrations are in the public domain. Following are original sources and accession of illustrations from Kerner  von Marilaun (1895); https://commons.wikimedia.org/wiki/File:Twining_Hop_(Humulus_lupulus).jpg. https://commons.wikimedia.org/wiki/

Commons:Reusing_content_outside_Wikimedia. b From Treub, (1883); http://www.amjbot.org/content/96/7/1205/F6.expansion. c From Britton and Brown (1913); https://plants.usda.gov/java/usageGuidelines?imageID=gaap2_001_avd.tif. https://plants.usda.gov/java/largeImage?imageID=gaap2_001_avd.tif. d From Darwin (1865); http://darwin-online.org.uk/converted/published/1865_plants_F834a.html

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Greater than one-third of all the seed plant families and three-quarters of all the eudicots contain species adapted to climb (Gianoli 2015b), indicating that the ability to climb has evolved many more times than originally hypothesized by Darwin (1865) and other authors in the nineteenth and twentieth centuries. The convergent evolution of climbing likely has been, at least, partially driven by physiological and environmental constraints dictating the biomechanical mode of attachment and climbing (Rowe et al. 2004; Lenaghan and Zhang 2012). Holding power is an obviously important adaptation in which plants have proven to be innovators. Plants use loops, hooks, and glue to get a grip. There are significant levels of attachment force–over three orders of magnitude (20 mN–20 N) (Table 1)—that are sufficient for vertical ascent and maintenance of position in various spe-cies and habitats. We see that root and tendril climbers that self-adhere to substrates by secreting glue are among the top species measured and studied for their holding force: Hedera helix L. (Araliaceae) (English ivy) (Endress and Thompson 1977; Steinbrecher et al. 2010; Melzer et al. 2012; Xia et al. 2011), Parthenocissus tricuspidata (Sieb. & Zucc,) Planch. (Vitaceae) (Boston ivy) (Steinbrecher et al. 2010; He et al. 2011), and Parthenocissus quinquefolia (L.) Plantch. (Vita-ceae) (Virginia creeper) (Steinbrecher et al. 2010).

Climbing strategies

Twining

Twining plants utilize helical stems to wrap around support structures and generate a “squeezing” force that prevents slippage down the support structure (Isnard et al. 2009) (Fig. 1a). The change in stem geometry can be predicted based upon the diameter of the supporting structure, with instability occurring as the radius of the support approaches the radius of curvature of the flexible stem apex-derived helix (Bell 1958; Silk and Hubbard 1991). After initial con-tact, the stem continues to expand from the apex, and a uni-form helix is formed (Silk and Hubbard 1991). To strongly

adhere to the surface, the helix is tightened around the sub-strate by twisting, bending, or stretching, but the biological mechanism is unknown. In the early stages of twining, the dominant force is frictional contact between the flexible api-cal region and the substrate, not the squeezing force that provides stability later in climbing. Generation of a frictional contact force by the flexible apical region has been impli-cated in the generation of the initial climbing force in many twining plants, such as the common morning glory, in which frictional forces generated are related to the diameter of the substrate (Bell 1958; Scher et al. 2001). Thicker substrates require a larger twining force than slender substrates, owing to the ability to form more gyres per unit length in the slen-der substrate compared to the thicker one (Scher et al. 2001).

One mechanism twiners use is modified flange-like stip-ules that extend from the base of petioles, as in the case of Dioscorea bulbifera L. (Dioscoreaceae) (air potato) and its relatives (Isnard et al. 2009). Despite relatively sparse dis-tribution along the stem, these stipules place the rigid basal portion of the stem under tension, and serve as the points-of-contact between the stem and the host or substrate (Isnard et al. 2009). It appears that other twining species, in diverse families, use structures that are homologous to air potato’s stipules. Some examples are stipules in Humulus lupulus L. (Cannabaceae) (hops), a curved petiole base in Phaseo-lus vulgaris L. (Fabaceae) (bean), and the pulvinate petiole twining representatives of the Menispermaceae (Isnard and Silk 2009).

Hook and leaf‑bearing climbing

While the stem plays a key role in twining, hook and leaf-bearing climbers employ a strategy in which specialized vegetative structures are used as the point of attachment. In the case of hook climbers, recurved spines, hooks, or thorns are used to passively assist the plant in climbing. These hooks are present on the plant during all stages of growth, whereby gravity assists support climbing by way of hooking the substrate without firmly attaching to it (Dar-win 1865). Leaf-bearers climb by way of touch-responsive

Table 1 Representative climbing plants and their attachment strengths as indicated by average values of maximum separation forces (+ standard deviation) the maximum force at failure (Fmax), if known

Structural category Scientific name Common name Attachment strength, Force (F) (substrate) References

Tendrils Parthenocissus tricuspidata Boston ivy 7.59 ± 2.53 N, Fmax = 14.03 N (plaster) Steinbrecher et al. (2010)Campsis radicans Trumpet vine 18.26 ± 6.00 N, Fmax = 25.18 N (wood) Steinbrecher et al. (2010)

Twining Dioscorea bulbifera Air potato 100–300 mN (squeezing force) Isnard et al. (2009)Ipomoea purpurea Morning glory 167 ± 46  mN (slender pole) Scher et al. (2001)

Adventitious roots Hedera helix English ivy 3.81 ± 2.41 N, Fmax = 7.07 N (bark) Steinbrecher et al. (2010)Hooks or thorns Galium aparine Cleaver 21.9 ± 13.4 mN adaxial leaf surface (foam plastic) Bauer et al. (2011)

33.3 ± 15.1 mN adaxial leaf surface (foam plastic) Bauer et al. (2011)

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structures (“irritable organs”) (Hemsley 1893) on leaves that undergo morphological changes after contacting a substrate. The physical anchors appear to be less prone to extreme mechanical stress and cannot be dislodged from a support by movement or mechanical failure, as observed in twining plants (Rowe and Isnard 2009).

One of the best studied examples of hook climbers are the climbing palms (Calamoideae and Araceae, e.g., Des-moncus), which utilize modified leaf apices (cirri) or inflo-rescences (flagella) that have recurved spines that indent into the surrounding host plants and other substrates (Cor-ner 1966; Isnard and Silk 2009; Rowe and Isnard 2009) (Fig. 1b). Larger plants tend to have larger hooks (Corner 1966; Dransfield 1978; Putz 1990). The hooks of climbing palms are oriented in the direction of least resistance and are capable of disengagement and reengagement as the climber becomes dislodged from its host (Putz 1990). While hooks tend to be durable with high mechanical strength (Putz 1990), senescence of organs with hooks can disrupt attach-ment (Isnard et al. 2009). Owing largely to the distribution of climbing palms, the hook climbers appear to be espe-cially frequently found in the tropics mid-latitudinal bands (Durigon et al. 2014).

Leaf-bearing climbers tend to have a proliferation of small hooks on leaves, as illustrated by Galium aparine (cleavers or catchweed bedstraw). This species uses modi-fied trichomes on both the abaxial and adaxial surfaces of the leaves to adhere to appropriate surfaces (Bowling et al. 2008; Bauer et al. 2011) (Fig. 1c). On the abaxial surface, the hooks are curved towards the leaf base and situated along the midrib and leaf margins with a lignified hollow struc-ture (Bauer et al. 2011; Andrews and Badyal 2014). On the adaxial surface, the hooks are smaller, oriented towards the leaf tip, and evenly distributed across the leaf surface (Bauer et al. 2011; Andrews and Badyal 2014). The difference in orientation of the hooks between the abaxial and adaxial surface allows the abaxial surface to “grab” the surround-ing leaves and substrates through frictional forces, while the reverse orientation on the adaxial surface reduces friction between the surrounding leaves. This results in the ability of the leaves to orient the adaxial surface of the leaves towards the sky to maximize photosynthesis, while attaching to suit-able substrates with the abaxial surface (Bowling et al. 2008; Bauer et al. 2011). In this way, the arrangement of hooks accommodates both photosynthesis and climbing. Another more complex example of leaf modifications for climbing can be found in Amphilophium crucigerum (L.) L.G. Lohm-ann (Bignoniaceae) (monkey’s comb). Herein, the initial growth of several nodes all with trifoliate leaves is followed by growth of complex leaves. These complex leaves are composed of a basal pair of foliate leaflets and bifurcated tendril-like leaflets (Seidelmann et al. 2012). When the soft hooks on the apical surface of the tendril-like leaflets

contact a substrate, they begin to differentiate into callus-like adhesive pads and form intimate contact with the substrate (Seidelmann et al. 2012). This intimate contact serves as a signal for the coiling of the tendril-like leaflet, which further brings the stem closer to the substrate, at which point the tissue lignifies (Seidelmann et al. 2012).

Tendril climbing

Tendrils are long, slender filamentous organs derived from stems, leaves or flower peduncles with spring-like growth upon contact stimuli (Jaffe and Galston 1968; Jaffe 1970a) (Fig. 1d). Such a tendril provides flexibility and resistance to high winds and weight-bearing loads (Jaffe 1970a). Ten-dril climbing was identified as the main mechanism of plant adaptation for climbing in two latitudinal bands (35% in 0°–5°, 41% in 20°–25°) in the Americas, and second high-est in all the other latitudinal bands (19–29%) (Gallagher and Leishman 2012). The prevalence of tendril climbing in the Americas may be attributed to species relatedness and the highly conserved traits among the relevant climbing plant taxa (Gallagher and Leishman 2012). In addition, tendril climbers appear to be especially prevalent in early succes-sional environments, forest edges, and in locations contain-ing diminutive host stems, thus indicating a potential limi-tation of this strategy (Gianoli 2015a). Elongated tendrils “search” for a substrate, after which “tip coiling” ensues at the point-of-contact. In some species, this initial coiling is followed by a secondary coiling termed “free coiling,” dur-ing which the tendrils contract spirally, which physically moves the climber closer to its host (Jaffe 1970b).

One example of a tendril coiling plant is Luffa cylindrica (L.) Roem. Cucurbitaceae (towel gourd). In the towel gourd, free tendrils most often form left-handed helices; however, when contact is made, the tendril gradually reverses direc-tion to form right-handed helices and wrap around a sub-strate (Wang et al. 2013). Mechanistically, the reversal in direction of the tendril coil is controlled by alternate shrink-ing and swelling of cells in the inner and outer layers of the tendril (Wang et al. 2013). In this way, deformation of the helical tendril can be derived from both the architecture and the mechanical properties of the cells, with hydraulic forces providing control over attachment (Wang et al. 2013) and subsequent free coiling, resulting in closer proximity to the host (Wang et al. 2013). In an apparent water conserva-tion strategy and given the high energy cost of generating these hydraulic forces, it is not surprising that tendrils will only undergo coiling upon contact with a surface (Jaffe and Galston 1968).

Some tendril climbers, such as Boston ivy and Vir-ginia creeper, secrete adhesive from tendrils for permanent attachment to substrates. Both of these species are charac-terized by tendrils that originate from shoots at the base

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of foliate leaves (Critchfield 1970; Yang and Deng 2013). The morphology of the tendril branches are markedly differ-ent, however, with bulbous, oval tendril tips in Boston ivy, and elongated, forked, cylindrical tapered tips in Virginia creeper (Wilson and Posluszny 2003). The tendrils repre-sent terminal extensions of the shoot, with their own lateral branches increasing the surface area of the tendril (Wilson and Posluszny 2003). In the event that a tendril contacts a surface, the tendril proceeds through a series of devel-opmental stages leading to permanent attachment with the surface and cell wall lignification (Junker 1976; Bowling and Vaughn 2009; Kim 2014).

Another example of adhesive-secreting tendril climb-ers are the passion flowers, Passiflora discophora P. Jørg. &Lawesson, Passiflora arbeliazii xx, and Passiflora tryph-ostematoides xx (Passifloraceae), which utilize attachment pads on branched tendrils to climb (Bohn et  al. 2015). While the majority of passion flowers climb using coiled tendrils, P. discophora climbs using multi-branched tendrils that emerge from the shoot and have adhesive pads on the

terminus of each tendril (Bohn et al. 2015). Similar to Par-thenocissus, attachment of P. discophora is a multistep pro-cess, utilizing intermittent contact prior to the formation of permanent attachment. While immature tendrils have a hook shape, similar to other tendril climbers, the tip adheres to the surface using epicuticular wax crystals (Bohn et al. 2015).

Root climbing

Root climbers use clusters of adventitious roots that emerge from internodes to climb a variety of substrates of various diameters, architectures, and texture (Fig. 2). While tendril climbers employ strategies that sometimes use both adhe-sive and non-adhesive secretions, all root climbers secrete an adhesive for attachment (Darwin 1865). When assess-ing their worldwide geographic importance, root climbers have the lowest species prominence across all the latitudes (Durigon et al. 2013). The habitat that appears to favor root climbers are wet forests with reduced seasonality and mesic high temperature extremes (Durigon et al. 2013).

Fig. 2 Participation of root hair in attachment strategy of English ivy. a SEM of root hair demonstrating point-of-contact between the secreted adhesive and the substrate. b SEM of root hair demonstrat-ing the helical from created upon lignification and dehydration. c, d Schematic of the process of dehydration and hook formation of a root

hair, further drawing the shoot into close contact with the substrate. Scale bar on overview 10 µm; scale bar on inset 5 µm. Modified from Melzer et  al. (2010), and reprinted with permission from the copy-right holder

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By far, the most studied example of a root climber is Eng-lish ivy (Melzer et al. 2012). The attachment of English ivy to natural and artificial substrates has been hypothesized to occur in a four-step process: initial physical contact with the substrate, intimate contact of the root with the substrate, chemical adhesion, and lignification with subsequent hook formation (Melzer et al. 2010) (Fig. 2). Using real-time video microscopy, it was observed that prior to attachment, adventitious roots elongate with the tips oriented in multi-ple directions (Melzer et al. 2012). After contact, root hairs begin to rapidly grow posteriorly to the root cap, and begin to secrete adhesive onto the attaching surface (Melzer et al. 2012; Lenaghan and Zhang 2012). While this is occurring, the adventitious root orients itself parallel to the substrate, bringing the root hairs into closer contact with the substrate and allowing the root hairs to penetrate into and bind to the substrate. Considering that each root hair is a single cell, elongation, vesicle formation, and secretion of the adhesive bears similarities to the papillate cells described for adhe-sive-secreting tendril climbers. It is believed that the root hairs use the secreted adhesive to form a strong initial bond with the surface, which is further strengthened when the root hair lignifies. Upon lignification, the root hair undergoes a drastic change in morphology, where the previously flexible linear structure becomes a rigid hook (Fig. 2). When the root hairs undergo this change, root hairs inserted into small crevices/pores in the surface will pull the adventitious root into even closer contact. The combination of this chemical and physical attachment process is believed to contribute to the high strength of adventitious root climbers to rough/porous substrates (Melzer et al. 2010) (Table 1). This phys-icochemical mechanism may also explain why English ivy has a limited ability to effectively attach to smooth surfaces, such as glass and aluminum, while Boston ivy has no such difficulty (Steinbrecher et al. 2010; Melzer et al. 2012). Cer-tainly, the molecular biology and biochemistry of climbing merits additional investigation.

Molecular and biochemical mechanisms of climbing via adhesion

Among the most flexible and strongest strategies for climb-ing is the use of plant-produced adhesives (Table 1). The strong interfacial bond between plant tissue and substrate generated by adhesive secreted by various plants discussed above motivated the elucidation of the adhesives’ chemis-try and biosynthesis. Boston ivy, as one example, secretes an adhesive primarily composed of mucopolysaccharides, including rhamnogalacturonan I (RGI), callose, and other mucilaginous pectins (Endress and Thompson 1976, 1977; Bowling and Vaughn 2008; He et al. 2011). Further analy-sis of the metallic components of the adhesive revealed the

presence of K+, Na+, Mg+, Fe, Mn, as well as Ca2+ (com-prising the highest concentration of these six elements) (He et al. 2011). Ca2+ may be of special importance, since it binds with high affinity to RGI (Bowling and Vaughn 2008; Scanlan et al. 2010; Yapo 2011). In other eukaryotic and prokaryotic adhesives, Ca2+ has been demonstrated as an important cross-linking co-factor to promote specific and non-specific binding to proteins and polysaccharides (Gee-sey et al. 2000). In this way, the presence of Ca2+ in the polysaccharide rich adhesive may indicate a conserved strat-egy for bioadhesives between plants and animals (Fant et al. 2002). Likewise, mushroom-shaped attachment appears to be the optimal geometry from a biological adhesive perspec-tive (Gorb and Varenburg 2007).

Passiflora uses a different chemistry in its adhesives com-pared to Boston ivy. Upon initial contact with the host, the plant triggers differentiation of epidermal cells at the apex into papillate cells, which are devoid of epicuticular wax (Bohn et al. 2015). These cells continue to grow and form a callus-like tissue (adhesive pad) that gradually fills the gaps between the pad and substrate, similar to the monkey’s comb (Bohn et al. 2015). Unlike the monkey’s comb, how-ever, an extracellular adhesive is secreted as the pad presses against the surface. The Passiflora adhesive is composed of cutin and lipids, with no mucopolysaccharides, callose, or proteins. After deposition of the adhesive, the adhesive pad collapses followed by lignification, which draws the tendril closer to the surface (Bohn et al. 2015). From this example, it can be seen that while the overall mechanism may be similar in adhesive tendril climbers, the adhesive is highly varied, which may have important evolutionary and structural implications.

In yet another example, English ivy utilizes adhesives that are nanocomposites composed of nanoparticles and a liquid polysaccharides matrix (Zhang et al. 2009; Xia et al. 2010, 2011). These nanoparticles are uniform 50–80 nm spheres that are associated with adhesive secreted by the root hairs during attachment (Zhang et al. 2009; Xia et al. 2010, 2011). Similar to that of Boston ivy adhesive, the nanoparticles are composed of C, N, S, and O, indicating that the nanoparticles are primarily composed of biological macromolecules (Lenaghan et al. 2013). Unlike the Boston ivy adhesive, however, no metals appear to be associated with the ivy nanoparticles indicating a key difference in the composite adhesives. Further research into the structure of the ivy nanoparticles revealed that the ivy nanoparticles were primarily composed of a glycoprotein complex (Lena-ghan et al. 2013). To determine if the nanoparticles alone could contribute to the adhesive strength of the ivy adhe-sive, a contact fracture mechanics model was tested, which determined van der Waals forces between the nanoparticles alone were not strong enough to produce the attachment strength observed experimentally (Wu et al. 2010). Based

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on this evidence, cross-linking between the nanoparticles and the polymer adhesive was hypothesized to be necessary for forming the strong bond between the root hairs and the contact surface. In this way, the overall mechanism of the Boston ivy and English ivy adhesives appears to be similar, with Ca2+ catalyzing cross-linking of the polysaccharides in the Boston ivy adhesive, and the ivy nanoparticles cross-linking the English ivy adhesive.

Current and potential bioinspired engineering applications from climbing plants

While numerous examples exist for the translation of animal-inspired climbing and attachment mechanisms to develop engineered products, few examples exist for the translation of plant-based climbing and attachment into other fields. A prime example of the translational success of an animal-inspired attachment process can be observed with the development of several mussel-inspired adhesives including Cell-Tak™ (reviewed in Silverman and Roberto 2007). Cell-Tak™ utilizes recombinant mussel adhesive proteins combined with synthetic polymers to fabricate an adhesive that can be used in medicine to ‘glue’ tissue together. Relative to mussel adhesive, the adhesives secreted from Boston ivy, English ivy, and Virginia creeper appear to have product development potential. The adhesive secreted by mussels is a composite composed of adhesive proteins, a polysaccharide matrix (collagen), and an enzyme (catechol oxidase) for cross-linking the two components. In the marine polychaete Phragmatopoma californica Kinberg (Polycheta, Sabellaridae), a similar adhesive is used to glue grains of sand together to form tubular dwellings; however, in this case, Ca2+ is used to cross-link adhesive proteins with the polysaccharide matrix (Stevens et al. 2007). Clearly, these two adhesives bear startling resemblance to the adhesives of Boston and English ivy, making both of these prime can-didates for translation into other fields, including biomedi-cine, paints, and synthetic adhesives. Further, a plant-based production system for adhesives and adhesive proteins has numerous advantages to animal-based systems. One of the greatest advantages is the ability to scale-up production of adhesive by adapting climbers as crops. For example, we have produced an initial horticultural production system for English ivy for nanoparticle biosynthesis (Burris et al. 2012), which would be amenable for scale-up.

Although it appears that liquid plant adhesives have reached just the premarket stage for commercial products, there are a few examples of plant-inspired dry adhesive, rely-ing on mechanical interlocking products on the market. The most successful example includes hook and loop enclosures, such as Velcro®, which was invented by George de Mestral

after he noticed Arctium sp. L. (Asteraceae) (burdock) fruit clinging to his pants. Velcro hooks are mimicked after the burdock hooks and the fabric part of the closure is a textile like his pants. His plants provided the loops. Recent research yielded hook enclosures based on the hooked trichomes of cleavers (Bauer et al. 2011).

In addition to hook and loop enclosure inventions inspired by plants, the robotics community has started to take note of the mechanics of attachment in climbing plants as a source of inspiration for grasping and climbing. One such example can be seen from the development of a kinematic model based on the tendrils of Passiflora (Vidoni et al. 2015). Here, tendril climbers inspired the investigation of using tendril-like smart materials in robotics. After simplification of the tendril mechanics, the researchers were able to pro-duce a prototype robot using “shape memory alloys”, actu-ating systems for coiling and pulling (Vidoni et al. 2015). Although these studies illustrate the feasibility of translating the mechanics of climbing and attachment in plants to real-world applications, there still exists a substantial deficit in research geared towards bioinspired engineering from climb-ing plants, at least relative to inventions inspired by animals.

Conclusions and future research directions

Future research on climbing plants might focus on sev-eral broad areas such as the genomics and biosynthesis of specialized cell exudates, cell wall specialization, and tendril architecture and hydraulics using plants them-selves. In this last area, hydraulic flow dynamics must be better understood to mimic the system or even adapt the system to other plants and devices. Clearly, the develop-ment of shape-changing alloys has opened the door for development of bioinspired tendril and twining systems. However, the robotic ‘tendrils’ produced by Vidoni et al. (2015) used heating and cooling for actuation. Might a better approach be an engineered plant, which controls an endogenous grasping function, but with a ‘reset’ but-ton? While at first blush, such a quest might seem imprac-tical or impossible. Nonetheless, plant species such as the Venus flytrap (Dionaea muscipula Sol. Ex J.Ellis, Droseraceae) and the sensitive plant (Mimosa pudica L. Fabaceae) naturally undergo rapid leaf movement followed by a slower movement to reset leaves to initial conditions. In these two (non-climbing) cases, movement is chemo-electrically actuated using thigmonastic movement, which is related to some climbing mechanisms in several ways (e.g., Burgert and Frazzl 2009). One aspect of particular interest is cell wall composition with regards to the wall architecture. Primary cell walls are primarily composed of polymers of cellulose, hemicelluloses and pectins, and cells can shrink or swell based on hydraulics imposed on

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these polymers (Burgert and Frazzi 2009). However, it is surprising that we still do not know the exact relation-ships among these polymers to one another in primary cell walls (much less secondary cell walls that additionally contain lignin), but our knowledge is increasing. Recently, Hesse et al. (2016) found notable lignification in climb-ing stems of the monocot Flagellaria indica yielding high flexural stiffness despite the lack of cambial tissue. Nishi-tani and Demura (2015) refer to plant cell walls as “intel-ligent frontiers capable of processing information from the environment and coordinating whole-plant growth by optimizing individual cell growth and differentiation.” Climbers appear to make differentiated and specialized cell walls, such as the case of cells surrounding and com-prising hooks (Gallenmüller et al. 2015). Given the recent attention to understanding the genomics and biochemistry of cell wall biosynthesis to understand how to make cellu-losic biofuels (Loque et al. 2015), it would not be beyond reason that we may someday engineer dynamic cell walls in climbing plants to perform various tasks.

Molecular biology and genomics of climbing plants might well accelerate the ‘low hanging fruit’ of bioin-spired products, adhesives. Plants have figured out numer-ous methods and polymers to secrete in terrestrial sys-tems for permanent and inexpensive attachment. Further research to understand the synthesis and secretion pathway could lead to the next generation of “green glue” grown from commodity crops such as maize, if not from the climbing plants themselves. Any plant genetic engineer-ing of this sort requires better understanding of the path-ways and signaling involved in generating and secreting the adhesive. It is apparent that it is a long climb to the top for using these fascinating plants for engineered products, but the economy of scale and push for renewable products should be motivation for development.

Author contribution statement JNB, together with SCL, provided a first draft that was further modified by CNS. All the authors are responsible for conceiving of the manuscript, its drafting and revisions.

Acknowledgements We thank the National Science Foundation CBET #0965877, the University of Tennessee, and the Ivan Racheff Chair of Excellence Endowment for funding. We appreciate interactions and stimulating conversations with Mingjun Zhang, an important contribu-tor to this field. We thank Victoria Brooks for rendering Figure 1. The authors also wish to thank two anonymous peer reviewers for their very helpful comments that resulted in a stronger paper.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflicts of interest.

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