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

REVIEW

Climbing : 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

Abstract Climbing 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- Despite the prolonged fascination with climbing plants, ized adaptations of climbing plants that enable them to com- we know surprisingly little about the molecular biology, pete for resources such as sunlight (Niklas 2011). Charles genomics and biochemistry of attachment and climbing Darwin (1865) first categorized climbing plants based on in plants. By way of contrast, we know much more about their modes of attachment: twining, hook and -bearers, the mechanisms that certain animals employ to adhere to tendril-bearers, and root climbers (Fig. 1). Thus, plants surfaces relative to that of climbing plants. For example, employ a diversity of strategies to use trees, bluffs, and various animal systems have been extensively characterized, now, human-created vertical structures to ‘cheat’ their way such as the attachment of marine invertebrates (e.g., Ben- to sunlight. Their ability to cheat is a function of physical edict and Picciano 1989; Lee et al. 2007; Lin et al. 2007; ‘engineering’ adaptations that are borne by largely unknown Sullan et al. 2009; Sangeetha et al. 2010) and the reversible biochemical and biosynthesis mechanisms. Ecologically, adhesion systems of multiple of arthropods, reptiles climbers are renowned for optimizing resource acquisition and amphibians (e.g., Artz et al. 2003; Huber et al. 2007; while minimizing costs from metabolism (Gianoli et al. Kesel et al. 2003, 2004; Autumn 2006). With the rise in 2012). nanotechnology research, plants appear to be falling even farther behind animals with regards to analyzing their attach- Communicated by Chun-Hai Dong. ment systems. Humans have a long history of ‘inventing-by-observation’ * C. Neal Stewart Jr. or copying innovations inspired by nature. Certainly, bioin- [email protected] spired engineering continues to gain footholds in the era of 1 Department of Sciences, University of Tennessee, systems and synthetic biology. Recent successes include the 2431 Joe Johnson Dr., Knoxville, TN 37996‑4561, USA translation of the fundamental principles of animal attach- 2 Department of Food Science, University of Tennessee, ment and climbing to robotics and adhesion (e.g., Awada Knoxville, TN 37996, USA et al. 2015; Kalouche et al. 2014; Palmer et al. 2009; San- 3 Department of Mechanical, Aerospace, and Biomedical tos et all. 2008; Seo et al. 2015; Gillies et al. 2013). We Engineering, University of Tennessee, Knoxville, TN 37996, should now take further advantage of the world of climbing USA

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Fig. 1 Species illustrating some of Darwin’s (1865) modes of climb- Commons:Reusing_content_outside_Wikimedia. b From Treub, ing. a Twiner Humulus lupulus, b hook climber Uncaria ovalifolia, (1883); http://www.amjbot.org/content/96/7/1205/F6.expansion. c c, leaf-bearer Galium aparine, d tendril-bearer dioica. These From Britton and Brown (1913); https://plants.usda.gov/java/usageG examples denote the wide range of adaptations of climbing among uidelines?imageID=gaap2_001_avd.tif. https://plants.usda.gov/java/ angiosperms. All the illustrations are in the public domain. Following largeImage?imageID=gaap2_001_avd.tif. d From Darwin (1865); are original sources and accession of illustrations from Kerner von http://darwin-online.org.uk/converted/published/1865_plants_F834a. Marilaun (1895); https://commons.wikimedia.org/wiki/File:Twining_ html Hop_(Humulus_lupulus).jpg. https://commons.wikimedia.org/wiki/ plants for their adhesive properties, materials, and other illustrated by two examples of how climbers uniquely cope innovations. with biotic and abiotic stress. The first example is Convol- In this paper, we will briefly review the modes of climb- vulus chilensis Pers. (Convolvulaceae) (correhuela), which ing as classified by botanists. These modes will note specific has evolved an elegant strategy in plant defense by climbing examples of plants to illustrate the diversity of climbing. onto cacti and thorny shrubs as a defense from mamma- Second, we will explore what is known about molecular and lian grazers (Atala and Gianoli 2008; Gonzales-Teuber and; biochemical mechanisms of climbing, with a focus on the Gianoli 2008). A second example is Ipomoea purpurea L. adhesives and nanoparticles. Finally, we will propose new (Roth) (Convolvulaceae) (common morning glory), which research directions as well as potential strategies to develop induces twining as an apparent response to snail herbivory bioinspired products. and drought conditions (Atala et al. 2014). Taxonomically, () are the most diverse climbers. When surveying 45 families of flowering plants, Evolution and taxonomic distribution 38 taxa of climbers had higher diversity compared with of climbing plants their non-climbing sister groups, which suggests that climb- ing was a key innovation to niche utilization, competition The ability to climb represents a diversity of biological inno- (Schweitzer and Larson 1999), and diversification (Gianoli vations to acquire physical space, nutrients, and especially 2004). Additionally, one kingdom-wide survey found that light, with minimal investment of resources by the climbing 171 plant families contain at least one climbing plant spe- plant (Rowe et al. 2004; Paul and Yavitt 2011; Biernaskie cies. They included nine families, two 2011; Gianolli 2004, 2015a). Certainly, the resource-effi- families, and families from three basal angiosperms, eight cient strategies used among species are divergent and can be magnoliids, 22 monocots and 127 (Gianoli 2015b).

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Greater than one-third of all the plant families and adhere to the surface, the helix is tightened around the sub- three-quarters of all the eudicots contain species adapted to strate by twisting, bending, or stretching, but the biological climb (Gianoli 2015b), indicating that the ability to climb mechanism is unknown. In the early stages of twining, the has evolved many more times than originally hypothesized dominant force is frictional contact between the flexible api- by Darwin (1865) and other authors in the nineteenth and cal region and the substrate, not the squeezing force that twentieth centuries. The convergent evolution of climbing provides stability later in climbing. Generation of a frictional likely has been, at least, partially driven by physiological and contact force by the flexible apical region has been impli- environmental constraints dictating the biomechanical mode cated in the generation of the initial climbing force in many of attachment and climbing (Rowe et al. 2004; Lenaghan twining plants, such as the common morning glory, in which and Zhang 2012). Holding power is an obviously important frictional forces generated are related to the diameter of the adaptation in which plants have proven to be innovators. substrate (Bell 1958; Scher et al. 2001). Thicker substrates Plants use loops, hooks, and glue to get a grip. There are require a larger twining force than slender substrates, owing significant levels of attachment force–over three orders of to the ability to form more gyres per unit length in the slen- magnitude (20 mN–20 N) (Table 1)—that are sufficient for der substrate compared to the thicker one (Scher et al. 2001). vertical ascent and maintenance of position in various spe- One mechanism twiners use is modified flange-like stip- cies and habitats. We see that root and tendril climbers that ules that extend from the base of petioles, as in the case of self-adhere to substrates by secreting glue are among the top Dioscorea bulbifera L. (Dioscoreaceae) (air potato) and its species measured and studied for their holding force: Hedera relatives (Isnard et al. 2009). Despite relatively sparse dis- helix L. (Araliaceae) (English ivy) (Endress and Thompson tribution along the stem, these stipules place the rigid basal 1977; Steinbrecher et al. 2010; Melzer et al. 2012; Xia et al. portion of the stem under tension, and serve as the points- 2011), Parthenocissus tricuspidata (Sieb. & Zucc,) Planch. of-contact between the stem and the host or substrate (Isnard (Vitaceae) (Boston ivy) (Steinbrecher et al. 2010; He et al. et al. 2009). It appears that other twining species, in diverse 2011), and Parthenocissus quinquefolia (L.) Plantch. (Vita- families, use structures that are homologous to air potato’s ceae) (Virginia creeper) (Steinbrecher et al. 2010). stipules. Some examples are stipules in Humulus lupulus L. (Cannabaceae) (hops), a curved base in Phaseo- lus vulgaris L. () (bean), and the pulvinate petiole Climbing strategies twining representatives of the Menispermaceae (Isnard and Silk 2009). Twining Hook and leaf‑bearing climbing Twining plants utilize helical stems to wrap around support structures and generate a “squeezing” force that prevents While the stem plays a key role in twining, hook and leaf- slippage down the support structure (Isnard et al. 2009) bearing climbers employ a strategy in which specialized (Fig. 1a). The change in stem geometry can be predicted vegetative structures are used as the point of attachment. based upon the diameter of the supporting structure, with In the case of hook climbers, recurved spines, hooks, or instability occurring as the radius of the support approaches thorns are used to passively assist the plant in climbing. the radius of curvature of the flexible stem apex-derived These hooks are present on the plant during all stages of helix (Bell 1958; Silk and Hubbard 1991). After initial con- growth, whereby gravity assists support climbing by way tact, the stem continues to expand from the apex, and a uni- of hooking the substrate without firmly attaching to it (Dar- form helix is formed (Silk and Hubbard 1991). To strongly 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 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)

1 3 568 Plant Cell Reports (2018) 37:565–574 structures (“irritable organs”) (Hemsley 1893) on that contact a substrate, they begin to differentiate into callus-like undergo morphological changes after contacting a substrate. adhesive pads and form intimate contact with the substrate The physical anchors appear to be less prone to extreme (Seidelmann et al. 2012). This intimate contact serves as a mechanical stress and cannot be dislodged from a support signal for the coiling of the tendril-like leaflet, which further by movement or mechanical failure, as observed in twining brings the stem closer to the substrate, at which point the plants (Rowe and Isnard 2009). tissue lignifies (Seidelmann et al.2012 ). One of the best studied examples of hook climbers are the climbing palms (Calamoideae and Araceae, e.g., Des- Tendril climbing moncus), which utilize modified leaf apices (cirri) or inflo- rescences (flagella) that have recurved spines that indent Tendrils are long, slender filamentous organs derived from into the surrounding host plants and other substrates (Cor- stems, leaves or flower peduncles with spring-like growth ner 1966; Isnard and Silk 2009; Rowe and Isnard 2009) upon contact stimuli (Jaffe and Galston 1968; Jaffe 1970a) (Fig. 1b). Larger plants tend to have larger hooks (Corner (Fig. 1d). Such a tendril provides flexibility and resistance 1966; Dransfield 1978; Putz 1990). The hooks of climbing to high winds and weight-bearing loads (Jaffe 1970a). Ten- palms are oriented in the direction of least resistance and are dril climbing was identified as the main mechanism of plant capable of disengagement and reengagement as the climber adaptation for climbing in two latitudinal bands (35% in becomes dislodged from its host (Putz 1990). While hooks 0°–5°, 41% in 20°–25°) in the Americas, and second high- tend to be durable with high mechanical strength (Putz est in all the other latitudinal bands (19–29%) (Gallagher and 1990), senescence of organs with hooks can disrupt attach- Leishman 2012). The prevalence of tendril climbing in the ment (Isnard et al. 2009). Owing largely to the distribution Americas may be attributed to species relatedness and the of climbing palms, the hook climbers appear to be espe- highly conserved traits among the relevant climbing plant cially frequently found in the tropics mid-latitudinal bands taxa (Gallagher and Leishman 2012). In addition, tendril (Durigon et al. 2014). climbers appear to be especially prevalent in early succes- Leaf-bearing climbers tend to have a proliferation of sional environments, forest edges, and in locations contain- small hooks on leaves, as illustrated by Galium aparine ing diminutive host stems, thus indicating a potential limi- (cleavers or catchweed bedstraw). This species uses modi- tation of this strategy (Gianoli 2015a). Elongated tendrils fied trichomes on both the abaxial and adaxial surfaces of “search” for a substrate, after which “tip coiling” ensues at the leaves to adhere to appropriate surfaces (Bowling et al. the point-of-contact. In some species, this initial coiling is 2008; Bauer et al. 2011) (Fig. 1c). On the abaxial surface, followed by a secondary coiling termed “free coiling,” dur- the hooks are curved towards the leaf base and situated along ing which the tendrils contract spirally, which physically the midrib and leaf margins with a lignified hollow struc- moves the climber closer to its host (Jaffe1970b ). ture (Bauer et al. 2011; Andrews and Badyal 2014). On the One example of a tendril coiling plant is Luffa cylindrica adaxial surface, the hooks are smaller, oriented towards the (L.) Roem. (towel gourd). In the towel gourd, leaf tip, and evenly distributed across the leaf surface (Bauer free tendrils most often form left-handed helices; however, et al. 2011; Andrews and Badyal 2014). The difference in when contact is made, the tendril gradually reverses direc- orientation of the hooks between the abaxial and adaxial tion to form right-handed helices and wrap around a sub- surface allows the abaxial surface to “grab” the surround- strate (Wang et al. 2013). Mechanistically, the reversal in ing leaves and substrates through frictional forces, while the direction of the tendril coil is controlled by alternate shrink- reverse orientation on the adaxial surface reduces friction ing and swelling of cells in the inner and outer layers of between the surrounding leaves. This results in the ability of the tendril (Wang et al. 2013). In this way, deformation of the leaves to orient the adaxial surface of the leaves towards the helical tendril can be derived from both the architecture the sky to maximize , while attaching to suit- and the mechanical properties of the cells, with hydraulic able substrates with the abaxial surface (Bowling et al. 2008; forces providing control over attachment (Wang et al. 2013) Bauer et al. 2011). In this way, the arrangement of hooks and subsequent free coiling, resulting in closer proximity to accommodates both photosynthesis and climbing. Another the host (Wang et al. 2013). In an apparent water conserva- more complex example of leaf modifications for climbing tion strategy and given the high energy cost of generating can be found in Amphilophium crucigerum (L.) L.G. Lohm- these hydraulic forces, it is not surprising that tendrils will ann () (monkey’s comb). Herein, the initial only undergo coiling upon contact with a surface (Jaffe and growth of several nodes all with trifoliate leaves is followed Galston 1968). by growth of complex leaves. These complex leaves are Some tendril climbers, such as Boston ivy and Vir- composed of a basal pair of foliate leaflets and bifurcated ginia creeper, secrete adhesive from tendrils for permanent tendril-like leaflets (Seidelmann et al. 2012). When the attachment to substrates. Both of these species are charac- soft hooks on the apical surface of the tendril-like leaflets terized by tendrils that originate from shoots at the base

1 3 Plant Cell Reports (2018) 37:565–574 569 of foliate leaves (Critchfield 1970; Yang and Deng 2013). terminus of each tendril (Bohn et al. 2015). Similar to Par- The morphology of the tendril branches are markedly differ- thenocissus, attachment of P. discophora is a multistep pro- ent, however, with bulbous, oval tendril tips in Boston ivy, cess, utilizing intermittent contact prior to the formation of and elongated, forked, cylindrical tapered tips in Virginia permanent attachment. While immature tendrils have a hook creeper (Wilson and Posluszny 2003). The tendrils repre- shape, similar to other tendril climbers, the tip adheres to the sent terminal extensions of the shoot, with their own lateral surface using epicuticular wax crystals (Bohn et al. 2015). branches increasing the surface area of the tendril (Wilson and Posluszny 2003). In the event that a tendril contacts Root climbing a surface, the tendril proceeds through a series of devel- opmental stages leading to permanent attachment with the Root climbers use clusters of adventitious roots that emerge surface and cell wall lignification (Junker 1976; Bowling and from internodes to climb a variety of substrates of various Vaughn 2009; Kim 2014). diameters, architectures, and texture (Fig. 2). While tendril Another example of adhesive-secreting tendril climb- climbers employ strategies that sometimes use both adhe- ers are the passion flowers, discophora P. Jørg. sive and non-adhesive secretions, all root climbers secrete &Lawesson, Passiflora arbeliazii xx, and Passiflora tryph- an adhesive for attachment (Darwin 1865). When assess- ostematoides xx (Passifloraceae), which utilize attachment ing their worldwide geographic importance, root climbers pads on branched tendrils to climb (Bohn et al. 2015). have the lowest species prominence across all the latitudes While the majority of passion flowers climb using coiled (Durigon et al. 2013). The habitat that appears to favor root tendrils, P. discophora climbs using multi-branched tendrils climbers are wet forests with reduced seasonality and mesic that emerge from the shoot and have adhesive pads on the high temperature extremes (Durigon et al. 2013).

Fig. 2 Participation of root hair in attachment strategy of English hair, further drawing the shoot into close contact with the substrate. ivy. a SEM of root hair demonstrating point-of-contact between the Scale bar on overview 10 µm; scale bar on inset 5 µm. Modified from secreted adhesive and the substrate. b SEM of root hair demonstrat- Melzer et al. (2010), and reprinted with permission from the copy- ing the helical from created upon lignification and dehydration.c, d right holder Schematic of the process of dehydration and hook formation of a root

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By far, the most studied example of a root climber is Eng- presence of ­K+, ­Na+, ­Mg+, Fe, Mn, as well as ­Ca2+ (com- lish ivy (Melzer et al. 2012). The attachment of English ivy prising the highest concentration of these six elements) (He to natural and artificial substrates has been hypothesized to et al. 2011). Ca­ 2+ may be of special importance, since it occur in a four-step process: initial physical contact with binds with high affinity to RGI (Bowling and Vaughn 2008; the substrate, intimate contact of the root with the substrate, Scanlan et al. 2010; Yapo 2011). In other eukaryotic and chemical adhesion, and lignification with subsequent hook prokaryotic adhesives, Ca­ 2+ has been demonstrated as an formation (Melzer et al. 2010) (Fig. 2). Using real-time important cross-linking co-factor to promote specific and video microscopy, it was observed that prior to attachment, non-specific binding to proteins and polysaccharides (Gee- adventitious roots elongate with the tips oriented in multi- sey et al. 2000). In this way, the presence of Ca­ 2+ in the ple directions (Melzer et al. 2012). After contact, root hairs polysaccharide rich adhesive may indicate a conserved strat- begin to rapidly grow posteriorly to the root cap, and begin egy for bioadhesives between plants and animals (Fant et al. to secrete adhesive onto the attaching surface (Melzer et al. 2002). Likewise, mushroom-shaped attachment appears to 2012; Lenaghan and Zhang 2012). While this is occurring, be the optimal geometry from a biological adhesive perspec- the adventitious root orients itself parallel to the substrate, tive (Gorb and Varenburg 2007). bringing the root hairs into closer contact with the substrate Passiflora uses a different chemistry in its adhesives com- and allowing the root hairs to penetrate into and bind to the pared to Boston ivy. Upon initial contact with the host, the substrate. Considering that each root hair is a single cell, plant triggers differentiation of epidermal cells at the apex elongation, vesicle formation, and secretion of the adhesive into papillate cells, which are devoid of epicuticular wax bears similarities to the papillate cells described for adhe- (Bohn et al. 2015). These cells continue to grow and form sive-secreting tendril climbers. It is believed that the root a callus-like tissue (adhesive pad) that gradually fills the hairs use the secreted adhesive to form a strong initial bond gaps between the pad and substrate, similar to the monkey’s with the surface, which is further strengthened when the root comb (Bohn et al. 2015). Unlike the monkey’s comb, how- hair lignifies. Upon lignification, the root hair undergoes a ever, an extracellular adhesive is secreted as the pad presses drastic change in morphology, where the previously flexible against the surface. The Passiflora adhesive is composed linear structure becomes a rigid hook (Fig. 2). When the of cutin and lipids, with no mucopolysaccharides, callose, root hairs undergo this change, root hairs inserted into small or proteins. After deposition of the adhesive, the adhesive crevices/pores in the surface will pull the adventitious root pad collapses followed by lignification, which draws the into even closer contact. The combination of this chemical tendril closer to the surface (Bohn et al. 2015). From this and physical attachment process is believed to contribute example, it can be seen that while the overall mechanism to the high strength of adventitious root climbers to rough/ may be similar in adhesive tendril climbers, the adhesive is porous substrates (Melzer et al. 2010) (Table 1). This phys- highly varied, which may have important evolutionary and icochemical mechanism may also explain why English ivy structural implications. has a limited ability to effectively attach to smooth surfaces, In yet another example, English ivy utilizes adhesives such as glass and aluminum, while Boston ivy has no such that are nanocomposites composed of nanoparticles and a difficulty (Steinbrecher et al. 2010; Melzer et al. 2012). Cer- liquid polysaccharides matrix (Zhang et al. 2009; Xia et al. tainly, the molecular biology and biochemistry of climbing 2010, 2011). These nanoparticles are uniform 50–80 nm merits additional investigation. 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 Molecular and biochemical mechanisms nanoparticles are composed of C, N, S, and O, indicating of climbing via adhesion that the nanoparticles are primarily composed of biological macromolecules (Lenaghan et al. 2013). Unlike the Boston Among the most flexible and strongest strategies for climb- ivy adhesive, however, no metals appear to be associated ing is the use of plant-produced adhesives (Table 1). The with the ivy nanoparticles indicating a key difference in the strong interfacial bond between plant tissue and substrate composite adhesives. Further research into the structure of generated by adhesive secreted by various plants discussed the ivy nanoparticles revealed that the ivy nanoparticles above motivated the elucidation of the adhesives’ chemis- were primarily composed of a glycoprotein complex (Lena- try and biosynthesis. Boston ivy, as one example, secretes ghan et al. 2013). To determine if the nanoparticles alone an adhesive primarily composed of mucopolysaccharides, could contribute to the adhesive strength of the ivy adhe- including rhamnogalacturonan I (RGI), callose, and other sive, a contact fracture mechanics model was tested, which mucilaginous pectins (Endress and Thompson 1976, 1977; determined van der Waals forces between the nanoparticles Bowling and Vaughn 2008; He et al. 2011). Further analy- alone were not strong enough to produce the attachment sis of the metallic components of the adhesive revealed the strength observed experimentally (Wu et al. 2010). Based

1 3 Plant Cell Reports (2018) 37:565–574 571 on this evidence, cross-linking between the nanoparticles after he noticed Arctium sp. L. (Asteraceae) (burdock) fruit and the polymer adhesive was hypothesized to be necessary clinging to his pants. Velcro hooks are mimicked after the for forming the strong bond between the root hairs and the burdock hooks and the fabric part of the closure is a textile contact surface. In this way, the overall mechanism of the like his pants. His plants provided the loops. Recent research Boston ivy and English ivy adhesives appears to be similar, yielded hook enclosures based on the hooked trichomes of with Ca­ 2+ catalyzing cross-linking of the polysaccharides cleavers (Bauer et al. 2011). in the Boston ivy adhesive, and the ivy nanoparticles cross- In addition to hook and loop enclosure inventions inspired linking the English ivy adhesive. 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 Current and potential bioinspired can be seen from the development of a kinematic model engineering applications from climbing based on the tendrils of Passiflora (Vidoni et al. 2015). plants Here, tendril climbers inspired the investigation of using tendril-like smart materials in robotics. After simplification While numerous examples exist for the translation of of the tendril mechanics, the researchers were able to pro- animal-inspired climbing and attachment mechanisms to duce a prototype robot using “shape memory alloys”, actu- develop engineered products, few examples exist for the ating systems for coiling and pulling (Vidoni et al. 2015). translation of plant-based climbing and attachment into Although these studies illustrate the feasibility of translating other fields. A prime example of the translational success the mechanics of climbing and attachment in plants to real- of an animal-inspired attachment process can be observed world applications, there still exists a substantial deficit in with the development of several mussel-inspired adhesives research geared towards bioinspired engineering from climb- including Cell-Tak™ (reviewed in Silverman and Roberto ing plants, at least relative to inventions inspired by animals. 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 Conclusions and future research directions together. Relative to mussel adhesive, the adhesives secreted from Boston ivy, English ivy, and Virginia creeper appear to Future research on climbing plants might focus on sev- have product development potential. The adhesive secreted eral broad areas such as the genomics and biosynthesis by mussels is a composite composed of adhesive proteins, a of specialized cell exudates, cell wall specialization, and polysaccharide matrix (collagen), and an enzyme (catechol tendril architecture and hydraulics using plants them- oxidase) for cross-linking the two components. In the marine selves. In this last area, hydraulic flow dynamics must be polychaete Phragmatopoma californica Kinberg (Polycheta, better understood to mimic the system or even adapt the Sabellaridae), a similar adhesive is used to glue grains of system to other plants and devices. Clearly, the develop- sand together to form tubular dwellings; however, in this ment of shape-changing alloys has opened the door for case, Ca­ 2+ is used to cross-link adhesive proteins with the development of bioinspired tendril and twining systems. polysaccharide matrix (Stevens et al. 2007). Clearly, these However, the robotic ‘tendrils’ produced by Vidoni et al. two adhesives bear startling resemblance to the adhesives (2015) used heating and cooling for actuation. Might a of Boston and English ivy, making both of these prime can- better approach be an engineered plant, which controls didates for translation into other fields, including biomedi- an endogenous grasping function, but with a ‘reset’ but- cine, paints, and synthetic adhesives. Further, a plant-based ton? While at first blush, such a quest might seem imprac- production system for adhesives and adhesive proteins has tical or impossible. Nonetheless, plant species such as numerous advantages to animal-based systems. One of the the Venus flytrap (Dionaea muscipula Sol. Ex J.Ellis, greatest advantages is the ability to scale-up production of Droseraceae) and the sensitive plant (Mimosa pudica L. adhesive by adapting climbers as crops. For example, we Fabaceae) naturally undergo rapid leaf movement followed have produced an initial horticultural production system by a slower movement to reset leaves to initial conditions. for English ivy for nanoparticle biosynthesis (Burris et al. In these two (non-climbing) cases, movement is chemo- 2012), which would be amenable for scale-up. electrically actuated using thigmonastic movement, which Although it appears that liquid plant adhesives have is related to some climbing mechanisms in several ways reached just the premarket stage for commercial products, (e.g., Burgert and Frazzl 2009). One aspect of particular there are a few examples of plant-inspired dry adhesive, rely- interest is cell wall composition with regards to the wall ing on mechanical interlocking products on the market. The architecture. Primary cell walls are primarily composed most successful example includes hook and loop enclosures, of polymers of cellulose, hemicelluloses and pectins, and such as Velcro®, which was invented by George de Mestral cells can shrink or swell based on hydraulics imposed on

1 3 572 Plant Cell Reports (2018) 37:565–574 these polymers (Burgert and Frazzi 2009). However, it References is surprising that we still do not know the exact relation- ships among these polymers to one another in primary cell Andrews HG, Badyal JPS (2014) Bioinspired hook surfaces based Galium aparine walls (much less secondary cell walls that additionally upon a ubiquitous weed ( ) for dry adhesion. J Adhesion Sci Technol 28:1243–1255 contain lignin), but our knowledge is increasing. Recently, Arzt E, Gorb S, Spolenak R (2003) From micro to nano contacts Hesse et al. (2016) found notable lignification in climb- in biological attachment devices. Proc Natl Acad Sci USA ing stems of the monocot Flagellaria indica yielding high 100:10603–10606 flexural stiffness despite the lack of cambial tissue. 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University of Cali- Excellence Endowment for funding. We appreciate interactions and fornia Press, Berkeley, p 393 stimulating conversations with Mingjun Zhang, an important contribu- Critchfield WB (1970) Shoot growth and leaf dimorphism in Boston tor to this field. We thank Victoria Brooks for rendering Figure 1. The ivy (Parthenocissus tricuspidata). Am J Bot 57:535–542 authors also wish to thank two anonymous peer reviewers for their very Darwin C (1865) On the movements and habits of climbing plants. helpful comments that resulted in a stronger paper. J Linn Soc Soc 9:1–118 Dransfield J (1978) Growth forms of rain forest palms, pp 247–268 in Compliance with ethical standards Tomlinson PB, Zimmermann MH (eds). 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