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Climbing Plants: Attachment Adaptations and Bioinspired Innovations

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Climbing Plants: Attachment Adaptations and Bioinspired Innovations 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 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 leaf-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 species 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 Plant 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 Vol.:(0123456789)1 3 566 Plant Cell Reports (2018) 37:565–574 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 Bryonia 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, vines (Vitaceae) 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 fern families, two gymnosperm 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 eudicots (Gianoli 2015b). 1 3 Plant Cell Reports (2018) 37:565–574 567 Greater than one-third of all the seed 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
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