How the Cucumber Tendril Coils and Overwinds

Gerbode, Sharon J.; Puzey, Joshua R.; McCormick, Andrew; Mahadevan, L.

doi:10.1126/science.1223304

Cited by 349 publications

(382 citation statements)

References 31 publications

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“…1A). Previous studies have emphasized mechanical strategies exploited by multiple climbing organs that evolve in plants (7)(8)(9)(10)(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).…”

mentioning

confidence: 99%

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

Huang

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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...

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mentioning

confidence: 99%

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

Huang

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…4G,H). As in nature, the result was equal numbers of coils of opposite handedness separated by a perversion point, as well as the overwinding of the coils when the two ends were pulled further apart (Gerbode et al, 2012).…”

Section: Tendrilsmentioning

confidence: 99%

“…Such fibres had been characterised in tension wood of flowering plants, where their contraction serves to straighten and lift growing branches (Goswami et al, 2008;Mellerowicz and Gorshkova, 2012). More recently, it was shown that in cucumber tendrils the gelatinous G-fibres occur as a bilayer of cells (Gerbode et al, 2012), with the layer closer to the inner, concave edge of the coil being ) A simplified model illustrating the dependence of the orientation of growing cellulose microfibrils within the developing cell wall on the pattern of underlying cortical microtubules. As multiple cellulose polymers are synthesised by the cellulose synthase rosette in the plasma membrane, they entwine in a microfibril that is embedded in the external cell wall.…”

Section: Tendrilsmentioning

confidence: 99%

“…(G) A G-fibre ribbon extracted from a cucumber tendril retains its coiled state, including a perversion point (arrow). E-G reproduced with permission from Gerbode et al (2012). (H) Proposed mechanism of coiling of a tendril by preferential contraction (dashed arrows) of the inner, more heavily lignified layer ( pale shading) of a gelatinous fibre ribbon in side view.…”

Section: Resupinationmentioning

confidence: 99%

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Helical growth in plant organs: mechanisms and significance

Smyth

2016

Development

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Many plants show some form of helical growth, such as the circular searching movements of growing stems and other organs (circumnutation), tendril coiling, leaf and bud reversal (resupination), petal arrangement (contortion) and leaf blade twisting. Recent genetic findings have revealed that such helical growth may be associated with helical arrays of cortical microtubules and of overlying cellulose microfibrils. An alternative mechanism of coiling that is based on differential contraction within a bilayer has also recently been identified and underlies at least some of these growth patterns. Here, I provide an overview of the genes and cellular processes that underlie helical patterning. I also discuss the diversity of helical growth patterns in plants, highlighting their potential adaptive significance and comparing them with helical growth patterns in animals.

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“…This salient feature of perversions accounts for several important observations, including the generation of more helices by a self-winding single perversion (6) and formation of the ripple patterns extensively found in animal guts and leaf edges through multiple perversions (18,19). Recent studies have further revealed that the perversion in the cucumber tendril, with its variable local stiffness, can unexpectedly overwind under tension rather than unwind (20). Previous theoretical studies using an ideal rod model with intrinsic curvature have qualitatively characterized the perversions (21,22), yet cannot fully capture the postbuckling deformation or the interactions between perversions.…”

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confidence: 99%

Emergent perversions in the buckling of heterogeneous elastic strips

Liu

Yao

Chiou

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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A perversion in an otherwise uniform helical structure, such as a climbing plant tendril, refers to a kink that connects two helices with opposite chiralities. Such singularity structures are widely seen in natural and artificial mechanical systems, and they provide the fundamental mechanism of helical symmetry breaking. However, it is still not clear how perversions arise in various helical structures and which universal principles govern them. As such, a heterogeneous elastic bistrip system provides an excellent model to address these questions. Here, we investigate intrinsic perversion properties which are independent of strip shapes. This study reveals the rich physics of perversions in the 3D elastic system, including the condensation of strain energy over perversions during their formation, the repulsive nature of the perversion-perversion interaction, and the coalescence of perversions that finally leads to a linear defect structure. This study may have implications for understanding relevant biological motifs and for use of perversions as energy storers in the design of micromuscles and soft robotics.S pontaneous symmetry breaking provides a unifying conceptual understanding of emergent ordered structures arising in various condensed matters (1). In an elastic medium, which is one of the simplest organizations of matter, symmetry-breaking instabilities via buckling can lead to extraordinarily rich patterns and generate a wealth of shapes at multiple length scales that can be exploited in many scientific disciplines (2). A prototype of elastic buckling is the Euler instability of a homogeneous elastic rod under uniaxial compression at the ends that finally breaks the rotational symmetry (3). Introduction of extra structures in an elastic medium like mechanical heterogeneities (4), nonlinearity of materials (2), geometric asymmetry (5), or intrinsic curvature (6) provides new dimensions that can produce even richer buckling modes, including helices and perversions (6, 7), wavy structures (8), regular networks of ridges (9), and even selfsimilar fractal patterns (2, 10). Of these emergent symmetry broken structures, the helical shapes are of particular interest due to their ubiquitousness in nature and the strong connection with biological motifs, as noticed by Darwin in his 1875 book describing the curl of plant tendrils (11). Remarkably, biological helical structures permeate over several length scales from the developed helical valve on opening seed pods (12), to the regular chiral structures in the flagella of bacteria (13), the spiral ramps of rough endoplasmic reticulum (14), and the chromosome of Escherichia coli (15, 16).The proliferation of perversions in an otherwise uniform helical structure can further break the helical symmetry (Fig. 1A shows a typical perversion in the helix) (4, 6, 17). Here, a perversion refers to a kink that connects two helices with opposite chiralities. Therefore, perversions belong to a large class of fundamental defects in systems with discrete symmetry which have the n...

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How the Cucumber Tendril Coils and Overwinds

Abstract: This copy is for your personal, non-commercial

Cited by 349 publications

References 31 publications

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

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

Helical growth in plant organs: mechanisms and significance

Emergent perversions in the buckling of heterogeneous elastic strips

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