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Plant Biomechanics pp 141–163Cite as

Plants at Bodybuilding: Development of Plant “Muscles”

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Abstract

Plant fibers are the important elements to shape the mechanical properties of plant body, especially in the organs that have already ceased elongation. The major distinguishing parameters of fibers are a highly prosenchimatous cell shape and an increased cell wall thickness as compared to other types of plant cells. The increase of fiber cell length is largely achieved by intrusive growth—elongation with the increased rate as compared to the adjacent cells and squeezing between them along the middle lamellae. The highly pronounced intrusive growth is the cause of fiber bundle formation. Thickening of cell wall in fibers of many plant species is supplied by deposition of the tertiary cell wall (G-layer) of peculiar design and properties. Tension of cellulose microfibrils is developed in this cell wall layer, providing the contractile properties that permit to move plant organs. We summarize the currently available data describing the inherent to fibers mechanisms by which they attain their exclusive length (intrusive growth) and extreme cell wall thickness (tertiary cell wall deposition) and consider the results obtained by finite element modeling to realize the cause of cellulose microfibril tension. The suggested hypothesis is based on the entrapment of tissue- and stage-specific version of rhamnogalacturonan I between laterally interacting cellulose microfibrils.

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References

  • Ageeva M, Petrovska B, Kieft H et al (2005) Intrusive growth of flax phloem fibres is of intercalary type. Planta 222:565–574

    Article  CAS  PubMed  Google Scholar 

  • Akin DE (2013) Linen most useful: perspectives on structure, chemistry, and enzymes for retting flax. ISRN Biotechnol 2013:186534

    Article  CAS  PubMed  Google Scholar 

  • Alméras T, Clair B (2016) Critical review on the mechanisms of maturation stress generation in trees. J R Soc Interface 13(122):20160550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bedinger PA, Hardeman KJ, Loukides CA (1994) Travelling in style: the cell biology of pollen. Trends Cell Biol 4:132–138

    Article  CAS  PubMed  Google Scholar 

  • Bos HL (2004) The potential of flax fibres as reinforcement for composite materials. Dissertation, Technische Universiteit Eindhoven

    Google Scholar 

  • Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burk DH, Liu B, Zhong R, Morrison WH, Ye Z-H (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13(4):807–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canaveze Y, Machado SR (2016) The occurrence of intrusive growth associated with articulated laticifers in Tabernaemontana catharinensis A.DC., a New Record for Apocynaceae. Int J Plant Sci 177(5):458–467

    Article  Google Scholar 

  • Cassan-Wang H, Goué N, Saidi MN et al (2013) Identification of novel transcription factors regulating secondary cell wall formation in Arabidopsis. Front Plant Sci 4:189

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang SS, Clair B, Ruelle J et al (2009) Mesoporosity as a new parameter for understanding tension stress generation in trees. J Exp Bot 60(11):3023–3030

    Article  CAS  PubMed  Google Scholar 

  • Chang SS, Quignard F, Almeras T, Clair B (2015) Mesoporosity changes from cambium to mature tension wood: a new step toward the understanding of maturation stress generation in trees. New Phytol 205(3):1277–1287

    Article  CAS  PubMed  Google Scholar 

  • Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube—spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160(4):1940–1955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernova TE, Gurjanov OP, Brach NB et al (2007) Variability in the composition of tissue-specific galactan from flax fibers. Russ J Plant Physiol 54(6):876–884

    Article  CAS  Google Scholar 

  • Chernova TE, Mikshina PV, Salnikov VV et al (2018) Development of distinct cell wall layers both in primary and secondary phloem fibers of hemp (Cannabis sativa L.). Ind Crop Prod 117:97–109

    Article  CAS  Google Scholar 

  • Clair B, Gril J, Di Renzo F et al (2008) Characterization of a gel in the cell wall to elucidate the paradoxical shrinkage of tension wood. Biomacromolecules 9:494–498

    Article  CAS  PubMed  Google Scholar 

  • Clair B, Alteyrac J, Gronvold A et al (2013) Patterns of longitudinal and tangential maturation stresses in Eucalyptus nitens plantation trees. Ann For Sci 70:801–811

    Article  Google Scholar 

  • Dadswell HE, Wardrop AB (1955) The structure and properties of tension wood. Holzforschung 9(4):97–104

    Article  CAS  Google Scholar 

  • Dawson C, Vincent JFV, Rocca A-M (1997) How pine cones open. Nature 390:668

    Article  CAS  Google Scholar 

  • Egholm RD, Christensen SF, Szabo P (2006) Stress-strain behavior in uniaxial compression of polymer gel beads. J Appl Polym Sci 102:3037–3047

    Article  CAS  Google Scholar 

  • Elbaum R, Zaltzman L, Burgert I, Fratzl P (2007) The role of wheat awns in the seed dispersal unit. Science 316(5826):884–886

    Article  CAS  PubMed  Google Scholar 

  • Esau K (1943) Vascular differentiation in the vegetative shoot of linum. III. The origin of the bast fibers. Am J Bot 30(8):579–586

    Article  Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. Wiley, New York

    Google Scholar 

  • Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley, New York

    Book  Google Scholar 

  • Fahn A (1990) Plant anatomy, 4th edn. Pergamon Press, Oxford

    Google Scholar 

  • Fan L-M, Wang Y-F, Wang H, Wu W-H (2001) In vitro Arabidopsis pollen germination and characterisation of the inward potassium currents in Arabidopsis pollen grain protoplasts. J Exp Bot 52:1603–1614

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A, Ortega JKE (2009) Mechanics and modeling of plant cell growth. Trends Plant Sci 14(9):467–478

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A (2016) Actuators acting without actin. Cell 166(1):15–17

    Article  CAS  PubMed  Google Scholar 

  • Gorshkov O, Mokshina N, Gorshkov V et al (2017) Transcriptome portrait of cellulose-enriched flax fibers at advanced stage of specialization. Plant Mol Biol 93:431–449

    Article  CAS  PubMed  Google Scholar 

  • Gorshkova TA, Wyatt SE, Salnikov VV et al (1996) Cell-wall polysaccharides of developing flax plants. Plant Physiol 110(2):721–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorshkova TA, Salnikov VV, Pogodina NM et al (2000) Composition and distribution of cell wall phenolic compounds in flax (Linum usitatissimum L.) stem tissues. Ann Bot 85(4):477–486

    Article  CAS  Google Scholar 

  • Gorshkova TA, Sal’nikov VV, Chemikosova SB et al (2003) The snap point: transition point in Linum usitatissimum L. bast fiber development. Ind Crops Prod 18:213–221

    Article  Google Scholar 

  • Gorshkova TA, Chemikosova SB, Salnikov VV et al (2004) Occurrence of cell-specific galactan is coinciding with bast fibre developmental transition in flax. Ind Crops Prod 19:217–224

    Article  CAS  Google Scholar 

  • Gorshkova T, Morvan C (2006) Secondary cell-wall assembly in flax phloem fibres: Role of galactans. Planta 223:149–158

    Article  CAS  PubMed  Google Scholar 

  • Gorshkova TA, Mikshina PV, Ibragimova NN et al (2009) Pectins in secondary cell walls: modifications during cell wall assembly and maturation. In: Schols HA, Visser RGF, Voragen AGJ (eds) Pectins and pectinases. Wageningen Academic Publishers, The Netherlands, pp 149–165

    Google Scholar 

  • Gorshkova TA, Gurjanov OP, Mikshina PV et al (2010) A special type of secondary cell wall, formed by plant fibers. Russ J Plant Physiol 57:346–361

    Article  CAS  Google Scholar 

  • Gorshkova T, Brutch N, Chabbert B et al (2012) Plant fibre formation: state of the art, recent and expected progress, and open questions. CRC Crit Rev Plant Sci 31:201–228

    Article  CAS  Google Scholar 

  • Gorshkova T, Mokshina N, Chernova T et al (2015) Aspen tension wood fibers contain β-(1 → 4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol 169(3):2048–2063

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gorshkova TA, Chernova TE, Gorshkov VY et al (2018) Intrusive growth of flax fibers: major players revealed by transcriptome analysis (in press)

    Google Scholar 

  • Gorshkova T, Chernova T, Mokshina N et al (2018) Plant “muscles”: fibers with a tertiary cell wall. New Phytol 218(1):66–72

    Article  CAS  PubMed  Google Scholar 

  • Goswami L, Dunlop JWC, Jungnikl K et al (2008) Stress generation in the tension wood of poplar is based on the lateral swelling power of the G-layer. Plant J 56:531–538

    Article  CAS  PubMed  Google Scholar 

  • Gray-Mitsumune M, Mellerowicz EJ, Abe H et al (2004) Expansins abundant in secondary xylem belong to subgroup A of the α-expansin gene family. Plant Physiol 135:1552–1564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray-Mitsumune M, Blomquist K, McQueen-Mason S et al (2008) Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol J 6:62–72

    PubMed  CAS  Google Scholar 

  • Guerriero G, Hausman J-F, Cai G (2014) No stress! Relax! Mechanisms governing growth and shape in plant cells. Int J Mol Sci 15:5094–5114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gurjanov OP, Gorshkova TA, Kabel MA et al (2007) MALDI-TOF MS evidence for the linking of flax bast fibre galactan to rhamnogalacturonan backbone. Carbohydr Polym 67:86–96

    Article  CAS  Google Scholar 

  • Gurjanov OP, Ibragimova NN, Gnezdilov OI, Gorshkova TA (2008) Polysaccharides, tightly bound to cellulose in the cell wall of flax bast fibre: Isolation and identification. Carbohydr Res 72:719–729

    Article  CAS  Google Scholar 

  • Hejnowicz Z (1980) Tensional stress in the cambium and its developmental significance. Am J Bot 67:1–5

    Article  Google Scholar 

  • Hepler PK, Winship LJ (2015) The pollen tube clear zone: clues to the mechanism of polarized growth. J Integr Plant Biol 57(1):79–92

    Article  CAS  PubMed  Google Scholar 

  • Hubbe MA (2006) Bonding between cellulosic fibers in the absence and presence of dry-strength agents. BioResources 1(2):281–318

    Google Scholar 

  • Ioelovich M (2008) Cellulose as a nanostructured polymer: a short. BioResources 3(4):1403–1418

    Google Scholar 

  • Jura-Morawiec J (2017) Atypical origin, structure and arrangement of secondary tracheary elements in the stem of the monocotyledonous dragon tree, Dracaena draco. Planta 245(1):93–99

    Article  CAS  PubMed  Google Scholar 

  • Larson PR (1994) The vascular cambium. Development and structure. Springer, Berlin

    Book  Google Scholar 

  • Lev-Yadun S (2001) Intrusive growth—the plant analog of dendrite and axon growth in animals. New Phytol 150:508–512

    Article  Google Scholar 

  • Lev-Yadun S, Dafni A, Flaishman MA et al (2004) Plant coloration undermines herbivorous insect camouflage. BioEssays 26:1126–1130

    Article  PubMed  Google Scholar 

  • Lev-Yadun S (2015) Plant development: cell movement relative to each other is both common and very important. Plant Sig Behav 10(3):e991566–1

    Article  CAS  Google Scholar 

  • Li WT, He M, Wang J, Wang YP (2013) Zinc finger protein (ZFP) in plants-a review. POJ 6(6):474–480

    CAS  Google Scholar 

  • Mazur E, Kurczynska EU (2012) Rays, intrusive growth, and storied cambium in the inflorescence stems of Arabidopsis thaliana (L.) Heynh. Protoplasma 249:217–220

    Article  CAS  PubMed  Google Scholar 

  • Mazur E, Kurczyńska EU, Friml J (2014) Cellular events during interfascicular cambium ontogenesis in inflorescence stems of Arabidopsis. Protoplasma 251:1125–1139

    Article  CAS  PubMed  Google Scholar 

  • Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:274–329

    Article  Google Scholar 

  • Mellerowicz EJ (2006) Xylem cell expansion—Lessons from poplar. In: Hayashi T (ed) The science and lore of the plant cell wall. Universal Publishers, Brown Walker Press, Boca Raton

    Google Scholar 

  • Mellerowicz EJ, Immerzeel P, Hayashi T (2008) Xyloglucan: the molecular muscle of trees. Ann Bot 102:659–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellerowicz EJ, Gorshkova TA (2012) Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. J Exp Bot 63:551–565

    Article  CAS  PubMed  Google Scholar 

  • Mikshina PV, Gurjanov OP, Mukhitova FK et al (2012) Structural details of pectic galactan from the secondary cell walls of flax (Linum usitatissimum L.) phloem fibres. Carbohydr Polym 87:853–861

    Article  CAS  Google Scholar 

  • Mikshina PV, Chernova TE, Chemikosova SB et al (2013) Cellulosic fibers: role of matrix polysaccharides in structure and function. In: van de Ven T, Godbout L (eds) Cellulose—fundamental aspects. InTech, Rijeka, pp 91–113

    Google Scholar 

  • Mikshina PV, Idiyatullin BZ, Petrova AA et al (2015a) Physicochemical properties of complex rhamnogalacturonan I from gelatinous cell walls of flax fibers. Carbohydr Polym 117:853–861

    Article  CAS  PubMed  Google Scholar 

  • Mikshina PV, Petrova AA, Idiyatullin BZ et al (2015b) Tissue-specific rhamnogalacturonan I forms the gel with hyperelastic properties. Biochem (Mosc) 80:915–924

    Article  CAS  Google Scholar 

  • Mikshina PV, Makshakova ON, Petrova AA et al (2017) Gelation of rhamnogalacturonan I is based on galactan side chain interaction and does not involve chemical modifications. Carbohydr Polym 171:143–151

    Article  CAS  PubMed  Google Scholar 

  • Mokshina NE, Ibragimova NN, Salnikov VV et al (2012) Galactosidase of plant fibers with gelatinous cell wall: identification and localization. Russ J Plant Physiol 59(2):246–254

    Article  CAS  Google Scholar 

  • Müller M, Burghammer M, Sugiyama J (2006) Direct investigation of the structural properties of tension wood cellulose microfibrils using microbeam X–ray fibre diffraction. Holzforschung 60:474–479

    Article  CAS  Google Scholar 

  • Nezhad AS, Geitmann A (2013) The cellular mechanics of an invasive lifestyle. J Exp Bot 64(15):4709–4728

    Article  CAS  Google Scholar 

  • Perez S, Mazeau K (2004) Conformations, structures, and morphologies of celluloses. In: Dumitriu S (ed) Polysaccharides, structure and functional versatility, 2nd edn. CRC Press, New York, pp 41–68

    Google Scholar 

  • Qin Y, Leydon AR, Manziello A et al (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5:e1000621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roach MJ, Mokshina NY, Badhan A et al (2011) Development of cellulosic secondary walls in flax fibers requires β-galactosidase. Plant Physiol 156(3):1351–1363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salnikov VV, Ageeva MV, Gorshkova TA (2008) Homofusion of Golgi secretory vesicles in flax phloem fibers during formation of the gelatinous secondary cell wall. Protoplasma 233:269–273

    Article  PubMed  Google Scholar 

  • Schreiber N, Gierlinger N, Pütz N et al (2010) G-fibres in storage roots of Trifolium pratense (Fabaceae): tensile stress generators for contraction. Plant J 61:854–861

    Article  CAS  PubMed  Google Scholar 

  • Siedlecka A, Wiklund S, Péronne M-A et al (2008) Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol 146:554–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snegireva AV, Ageeva MV, Vorob’ev VN et al (2006) Plant fiber intrusive growth characterized by NMR method. Russ J Plant Physiol 53:163–168

    Article  CAS  Google Scholar 

  • Snegireva A, Ageeva M, Amenitskii S et al (2010) Intrusive growth of sclerenchyma fbers. Russ J Plant Physiol 57:342–355

    Article  CAS  Google Scholar 

  • Snegireva A, Chernova T, Ageeva M et al (2015) Intrusive growth of primary and secondary phloem fibres in hemp stem determines fibre-bundle formation and structure. AoB Plants 7:plv061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturcova A, His I, Apperley DC et al (2004) Structural details of crystalline cellulose from higher plants. Biomacromol 5:1333–1339

    Article  CAS  Google Scholar 

  • Viëtor RJ, Newman RH, Ha MA et al (2002) Conformational features of crystal-surface cellulose from higher plants. Plant J 30:721–731

    Article  Google Scholar 

  • Wang Y, Zhang WZ, Song LF et al (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SS, Diao WZ, Yang X et al (2015) Arabidopsis thaliana CML25 mediates the Ca(2 +) regulation of K(+) transmembrane trafficking during pollen germination and tube elongation. Plant Cell Environ 38(11):2372–2386

    Article  CAS  PubMed  Google Scholar 

  • Wenham MW, Cusick F (1975) The growth of secondary wood fibres. New Phytol 74:247–261

    Article  Google Scholar 

  • Yamamoto H, Ruelle J, Arakawa Y et al (2010) Origin of the characteristic hygro-mechanical properties of the gelatinous layer in tension wood from Kunugi oak (Quercus acutissima). Wood Sci Technol 44:149–163

    Article  CAS  Google Scholar 

  • Yang Zh (1998) Signaling tip growth in plants. Curr Opin Plant Biol 1:525–530

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ye Zh-H (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomainleucine zipper protein. Plant Cell 11:2139–2152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Burk DH, Ye ZH (2001) Fibers. A model for studying cell differentiation, cell elongation, and cell wall biosynthesis. Plant Physiol 126(2):477–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Demura T, Ye Zh-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18(11):3158–3170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Ye Zh-H (2014) Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci 229:193–207

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann U, Husken D, Schulze ED (1980) Direct turgor pressure measurements in individual leaf cells of Tradescantia virginiana. Planta 149:445–453

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study was supported by Russian Science Foundation (project 16-14-10256—GT, CT, MN, GO; comparison of sets of genes up-regulated in intrusively elongating fibers and growing in vitro pollen tube; analysis of post-deposition modification of tertiary cell wall), and Program of the President of Russian Federation for Young Scientists (project MK-8393.2016.4—MP; analysis of the rhamnogalacturonan I ability to gelation and finite element modeling of tension creation in tertiary cell wall; project MK-8014.2016.4—PA, MN; study of the tissue-specific galactosidase role in the gelatinous cell wall formation).

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Authors and Affiliations

  1. The Laboratory of Plant Cell Growth Mechanisms, Kazan Institute of Biochemistry and Biophysics, FRC Kazan Scientific Center of RAS, 420111, Kazan, Russia

    Tatyana Gorshkova, Polina Mikshina, Anna Petrova, Tatyana Chernova, Natalia Mokshina & Oleg Gorshkov

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  1. Tatyana Gorshkova
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  2. Polina Mikshina
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  3. Anna Petrova
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  4. Tatyana Chernova
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  5. Natalia Mokshina
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  6. Oleg Gorshkov
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Correspondence to Tatyana Gorshkova .

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Editors and Affiliations

  1. Faculty of Agricultural and Environmental Sciences, McGill University, Macdonald Campus, Sainte-Anne-de-Bellevue, Québec, Canada

    Anja Geitmann

  2. CNRS, Université Clermont Auvergne, SIGMA Clermont, Institut Pascal, Clermont-Ferrand, France

    Joseph Gril

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Gorshkova, T., Mikshina, P., Petrova, A., Chernova, T., Mokshina, N., Gorshkov, O. (2018). Plants at Bodybuilding: Development of Plant “Muscles”. In: Geitmann, A., Gril, J. (eds) Plant Biomechanics. Springer, Cham. https://doi.org/10.1007/978-3-319-79099-2_7

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