Plant Biomechanics: Using Shape toSteal Motion

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  • Dispatchand seemingly hope for the best. Arecent paper by Kulic et al. [1] showsthat some grasses, at least, are not socavalier and have engineered theirseed carrying appendages (spikelets)to increase dispersion and facilitateseed burial by converting periodic orrandom oscillations in the environmentinto directed motion.

    The spatial extent of a plantpopulation is largely determined byseed dispersal [2]. There are three main

    DExperience-dependent modulation ofC. elegans behavior by ambient oxygen.Curr. Biol. 15, 905917.

    7. Zimmer, M., Gray, J.M., Pokala, N., Chang, A.J.,Karrow, D.S., Marletta, M.A., Hudson, M.L.,Morton, D.B., Chronis, N., and Bargmann, C.I.(2009). Neurons detect increases anddecreases in oxygen levels usingdistinct guanylate cyclases. Neuron 61,865879.

    8. Hoogewijs, D., De Henau, S., Dewilde, S.,Moens, L., Couvreur, M., Borgonie, G.,Vinogradov, S.N., Roy, S.W., and

    Plant Biomechanicto Steal Motion

    For grass species to spread efficientlyseeds that can disperse over large distRecent work using awns from Hordeummathematical modelling shows that awoscillations in order to produce these d

    Charles W. Wolgemuth

    Vince Guaraldi, the jazz pianist andcomposer, suggested with a songtitle that we should cast our fates tothe wind. As animals, though, weare typically not so trusting of thebenevolence of Nature and, instead,decide where we want to go andexpend energy to move there. Manyplants nevertheless release their seeds

    R409mechanisms for seed dispersal: beingcarried by the wind, water, or an animal.Foxtail grasses employ a spikelet orcluster of spikelets that contains thegrass seeds. These spikelets areengineered for hitch-hiking on animals.The more entrapped a spikeletbecomes in an animals fur, the fartherthe animal can carry the seed, and,therefore, it is beneficial for the spikeletto work its way into an animals coat.Kulic et al. [1] used scanning electronmicroscopy to show that the awn froman H. murinum spikelet has sharpmicro-barbs that are angled at roughlywhen pushed along one direction,

    A BStick

    Figure 1. How foxtail grass seeds steal motio

    (A) A cluster of spikelets has the appearancefrom H. murinum. The long arms that projectelectron microscopy shows that the awn suWhen a spikelet is placed on a shaking surfacone direction, and the spikelet moves with thother direction, the spikelet continues moving iwith the surface.show that anisotropic friction is

    C

    EVanfleteren, J.R. (2008). TheCaenorhabditis globin gene familyreveals extensive nematode-specificradiation and diversification. BMC Evol.Biol. 8, 279.

    9. Hoogewijs, D., Geuens, E., Dewilde, S.,Vierstraete, A., Moens, L., Vinogradov, S., andVanfleteren, J.R. (2007). Wide diversity instructure and expression profiles amongmembers of the Caenorhabditis elegans globinprotein family. BMC Genomics 8, 356.

    10. Rockman, M.V., and Kruglyak, L. (2009).Recombinational landscape and population

    genomics of Caenorhabditis elegans. PLoSGenet. 5, e1000419.

    Department of Neurobiology, Universityof Massachusetts Medical School,364 Plantation Street, Worcester,MA 01605, USA.E-mail: Mark.Alkema@umassmed.edu

    DOI: 10.1016/j.cub.2009.03.058

    s: Using Shape

    through their environment requiresances and burrow into the ground.murinum in conjunction withn shape leverages environmentalirectional translations.

    35 with respect to the awn (Figure 1).These micro-barbs produceanisotropic friction with theenvironment [1]. The awn slides easily

    but when pushed in the otherdirection, the barbs catch.

    The barbs thus act as ratchets,allowing motion in one direction andpreventing the counter motion. Ifa spikelet is placed on a rough surfacethat is shaken at a fixed frequency, thebarbs slip with respect to the surfacewhen the surface moves one way, butstay stuck to the surface when it movesin the other direction, which leads tonet motion of the spikelet (Figure 1).Using a simple mathematical modelthat incorporates this sticking andslipping, Kulic et al. [1] were able toSlipCurrent Biology

    n from the environment.

    of a foxtail. (B) Schematic of a single spikeletoff the base are known as awns. (C) Scanningrface is covered with angled micro-barbs. (D)e, the barbs catch when the surface moves ine surface. (E) When the surface moves in then the original direction, but slows due to friction

  • all of these examples, the moleculesratchet random motions from thermalfluctuations and thereby drive manyprocesses in our cells. New workalso suggests that jelly fish and somebugs may be able to steal motionfrom undulating water or air currents:Spagnolie and Shelley [7] have shownthat if a swimmer, such as a jelly fish,changes its shape out of step witha periodic flow, it can swim.

    Biology has thus repeatedly foundways of producing net work byrectifying fluctuations with ratchets,and it is interesting to speculate onother areas where this mechanism mayplay a role. Evolution is one directlyanalogous system and a comparisonbetween it and Brownian ratchetshas been drawn previously [8]. Clearly,random mutations in an organismsgenome lead to fluctuations inphenotype. Reproduction can lock in

    trapping useful ideas from a pool ofnoise? One of the not-so-useful ideas,right? But, it has been suggestedthat certain nuclei in the basalganglia act as a random motorpattern noise generator [9]. If ourbrains can create noise, maybe theycan ratchet it too.

    References1. Kulic, I.M., Mani, M., Mohrbach, H., Thaokar, R.,

    and Mahadevan, L. (2009). Botanicalratchets. Proc. Roy. Soc. Lond. B., epubahead of print.

    2. Garcia, D., Rodriquez-Cabal, M.A., andAmico, G.C. (2009). Seed dispersal by afrugivorous marsupial shapes the spatial scaleof a mistletoe population. J. Ecology 97,217229.

    3. Garnier, L.K.M., and Dajoz, I. (2001). Evolutionarysignificance of awn length variation in a clonalgrass of fire-prone savannas. Ecology 82,17201733.

    4. Murbach, L. (1900). Note on the mechanics of theseed-burying awns of Stipa avenacea. BotanicalGazette 30, 113117.

    5. Hazel, J., Stone, M., Grace, M.S., andTsukruk, V.V. (1999). Nanoscale design of snakeskin for reptation locomotions via friction

    Current Biology Vol 19 No 10sufficient to explain the net translationof the spikelet as a function of theapplied frequency. So when thespikelet is in contact with an animalsfur, random motions of the animal canlead to the ratcheting of the spikeletfurther into the animals coat.

    Spikelets also use this mechanismto facilitate burying themselves intothe ground, which acts not only toplant the seeds, but also to protectthe grass species during fires [3].Periodic variation in humidity causessoil swelling and leads to changes inawn shape [4]. To model how theanisotropic friction of grass awnscouples to soil swelling, Kulic et al. [1]inserted grass spikelets into a rubbertube. The tube was then slowlystretched and relaxed and the motionof the spikelet with respect to the tubewas measured [1]. Kulic et al. [1]developed a mathematical model thatdescribes how these changes inenvironmental strain the stretchingof the environment can interact withthe spikelet in order to bury the seeds.The model predicts that the burial rateshould increase with environmentalstrain and with awn length. This latterprediction is in good agreement withmeasurements of the burial depth ofStipa somata awns as a function ofawn length [3]. Some awns also havea twisted shape at the end, whichcan facilitate burying [4].

    Grass awns are not the only placewhere biology has found a use forcoupling anisotropic friction toundulatory motion in order to createnet translation. Another prime exampleof this mechanism is the motility ofsnakes and earthworms. Snake skinhas slanted micro-hairs [5], analogousto the micro-barbs observed in awns,and these micro-hairs lead tosignificant frictional anisotropybetween forward and backwardmotions [6]. Contraction and extensionof the snake musculature produces anoscillatory motion of the snake skinagainst the surface, and the combinedeffect gives a slithering snake.

    An interesting difference betweenthe snake and the awn is that the snakerelies on its own power, while the awneffectively steals energy from theenvironment. Biology has figured thisstrategy out in other arenas, too. Insidecells, some proteins can do work. Amyosin molecule walks to pull on actinand contract muscle. Actin, itself, canpolymerize and push. The flagellar

    R410motor and ATP synthase rotate. Forthese variations, and natural selectionthen acts as a ratchet, reducing thelikelihood of maintaining a populationthat is less competent at reproducingwhile increasing phenotypicpopulations that are fitter. A moretenuous comparison, though, comesto mind when I consider my ownthoughts, which all too often seemquite random. I must consciouslywork to rectify these thoughts, pluckingout the good ones and discarding thebad, in an attempt to construct anunderstanding of the world about me.Could my own thinking be working by

    Nuclear Envelope:Bending for Pore F

    Membrane-shaping proteins known asendoplasmic reticulum; recent findingsformation of nuclear-pore-complex-as

    Wolfram Antonin

    In eukaryotic cells, nuclear porecomplexes (NPCs) in the nuclearenvelope mediate transport betweenthe cytoplasm and the nucleoplasm.These are huge macromolecularassemblies of about 65 MDa in yeastand up to 120 MDa in vertebrates.Although most, if not all, componentsof NPCs are known [1,2], it is not fully

    understood how these large structuresanisotropy. J. Biomech. 32, 477484.6. Gray, J., and Lissmann, H.W. (1950). The kinetics

    of locomotion of the grass snakes. J. Exp. Biol.26, 354367.

    7. Spagnolie, S.E., and Shelley, M.J. (2009). Shape-changing bodies in fluid: hovering, ratcheting,and bursting. Phys. Fluids 21, 013103.

    8. Oster, G. (2002). Darwins motors. Nature 417, 25.9. Llinas, R. (2001). I of the Vortex: From Neurons to

    Self (Cambridge: MIT Press).

    University of Connecticut Health Center,Department of Cell Biology and Center forCell Analysis and Modeling, Farmington,CT 06030-3505, USA.E-mail: cwolgemuth@uchc.edu

    DOI: 10.1016/j.cub.2009.03.052

    Membraneormation?

    reticulons help to sculpt theindicate that they also play a role in thesociated pores in the nuclear envelope.

    are formed from their individualproteins. Nevertheless, significantprogress in understanding the proteininteraction network in the NPC hasbeen made in recent years [3,4].NPCs are embedded in the membraneof the nuclear envelope, but howinsertion is achieved is not known [5].An inspiring new study [6] suggeststhat the membrane bending proteinsof the endoplasmic reticulum (ER)

    play a role in this process.

    Plant Biomechanics: Using Shape toSteal MotionReferences