Skip to main content
Log in

Development of gravitropic response: unusual behavior of flax phloem G-fibers

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The major mechanism of gravitropism that is discussed for herbal plants is based on the nonuniform elongation of cells located on the opposite stem sides, occurring in the growing zone of an organ. However, gravitropic response of flax (Linum usitatissimum L.) is well-pronounced in the lower half of developing stem, which has ceased elongation long in advance of plant inclination. We have analyzed the stem curvature region by various approaches of microscopy and found the undescribed earlier significant modifications in primary phloem fibers that have constitutively developed G-layer. In fibers on the pulling stem side, cell portions were widened with formation of “bottlenecks” between them, leading to the “sausage-like” shape of a cell. Lumen diameter in fiber widening increased, while cell wall thickness decreased. Callose was deposited in proximity to bottlenecks and sometimes totally occluded their lumen. Structure of fiber cell wall changed considerably, with formation of breaks between G- and S-layers. Thick fibrillar structures that were revealed in fiber cell wall by light microscopy got oblique orientation instead of parallel to the fiber axis one in control plants. The described changes occurred at various combinations of gravitational and mechanical stimuli. Thus, phloem fibers with constitutively formed gelatinous cell wall, located in nonelongating parts of herbal plant, are involved in gravitropism and may become an important element in general understanding of the gravity effects on plants. We suggest flax phloem fibers as the model system to study the mechanism of plant position correction, including signal perception and transduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ageeva MV, Petrovska B, Kieft H, Salnikov VV, Snegireva AV, Van Dam JEG, Van Veenendaal WLH, Emons AMC, Gorshkova TA, Van Lammeren AAM (2005) Intrusive growth of flax phloem fibers is of intercalary type. Planta 222:565–574

    Article  CAS  PubMed  Google Scholar 

  • Aldaba VC (1927) The structure development the cell wall in plants I. Bast fibers Boehmeria Linum. Am J Bot 14:16–22

    Article  Google Scholar 

  • Altaner CM, Tokareva EN, Jarvis MC, Harris PJ (2010) Distribution of (1 → 4)-β-galactans, arabinogalactan proteins, xylans and (1 → 3)-β-glucans in tracheid cell walls. Tree Physiol 30:782–793

    Article  CAS  PubMed  Google Scholar 

  • Anderson AC, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Am J Plant Physiol 152:787–796

    Article  CAS  Google Scholar 

  • Belova NA, Lednev VV (2001) Activation and inhibition of the gravitropic response in the flax stem segments exposed to the permanent magnetic field with magnetic density ranging from 0 to 350 microTesla. Biofizika 46:118–121

    CAS  PubMed  Google Scholar 

  • Bowling AJ, Vaughn KC (2009) Gelatinous fibers are widespread in coiling tendrils and twining vines. Am J Bot 96:719–727

    Article  PubMed  Google Scholar 

  • Clair B, Alméras T, Pilate G, Jullien D, Sugiyama J, Riekel C (2011) Maturation stress generation in poplar tension wood studied by synchrotron radiation microdiffraction. Plant Physiol 155:562–570

    Article  CAS  PubMed  Google Scholar 

  • Dardelle F, Lehner A, Ramdani Y, Bardor M, Lerouge P, Driouich A, Mollet J-C (2010) Biochemical and immunocytological characterizations of arabidopsis pollen tube cell wall. Am J Plant Physiol 153:1563–1576

    Article  CAS  Google Scholar 

  • Day A, Ruel K, Neutelings G, Crônier D, David H, Hawkins S, Chabbert B (2005) Lignification in the flax stem: evidence for an unusual lignin in bast fibers. Planta 222:234–245

    Article  CAS  PubMed  Google Scholar 

  • Donaldson L (2007) Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci Technol 41:443–460

    Article  CAS  Google Scholar 

  • Donaldson L (2008) Microfibril angle: measurement, variation and relationships—a review. IAWA J 29:345–386

    Article  Google Scholar 

  • Eschrich W, Currier HB (1964) Identification of Callose by its Diachrome and Fluochrome Reactions. Stain Technol 39:303–307

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Fang CH, Clair B, Gril J, Liu SQ (2008) Growth stresses are highly controlled by the amount of G-layer in poplar tension wood. IAWA J 29:237–246

    Article  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubus and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Fisher JB (2008) Anatomy of axis contraction in seedlings from a fire prone habitat. Am J Bot 95:1337–1348

    Article  PubMed  Google Scholar 

  • Fisher JB, Blanco MA (2014) Gelatinous fibers and variant secondary growth related to stem undulation and contraction in a monkey ladder vine, Bauhinia glabra (Fabaceae). Am J Bot 101:608–616

    Article  PubMed  Google Scholar 

  • Gerbode SJ, Puzey JR, McCormick AG, Mahadevan L (2012) How the cucumber tendril coils and overwinds. Science 337:1087–1091

    Article  CAS  PubMed  Google Scholar 

  • Gorshkova TA, Wyatt SE, Salnikov VV, Gibeaut DM, Ibragimov MR, Lozovaya VV, Carpita N (1996) Cell wall polysaccharides of developing flax plants. Plant Physiol 110:721–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorshkova TA, Salnikov VV, Chemikosova SB, Ageeva MV, Pavlencheva NV, Van Dam JEG (2003) The snap point: a transition point in Linum usitatissimum bast fiber development. Ind Crop Prod 18:213–221

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gorshkova TA, Gurjanov OP, Mikshina PV, Ibragimova NN, Mokshina NE, Salnikov VV, Ageeva MV, Amenitskii SI, Chernova TE, Chemikosova SB (2010) Specific type of secondary cell wall formed by plant fibers. Russ J Plant Physiol 57:328–341

    Article  CAS  Google Scholar 

  • Gorshkova T, Brutch N, Chabbert B, Deyholos M, Hayashi T, Lev-Yadun S, Mellerowicz EJ, Morvan C, Neutelings G, Pilate G (2012) Plant fiber formation: state of the art, recent and expected progress, and open questions. Crit Rev Plant Sci 31:201–228

    Article  CAS  Google Scholar 

  • Gorshkova T, Mokshina N, Chernova N, Ibragimova N, Salnikov V, Mikshina P, Tryfona T, Banasiak A, Immerzeel P, Dupree P, Mellerowicz EJ (2015) Aspen tension wood fibers contain β-(1 → 4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls. Plant Physiol 169:2048–2063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goswami L, Dunlop JWC, Jungnikl K, Eder M, Gierlinger N, Coutand C, Jeronimidis G, Fratzl P, Burgert I (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 

  • Gurjanov OP, Gorshkova TA, Kabel M, Schols HA, van Dam JEG (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 cell wall of flax bast fibre: isolation and identification. Carbohydr Polym 72:719–729

    Article  CAS  Google Scholar 

  • Hasenstein KH (2009) Plant responses to gravity – insights and extrapolations from ground studies. Gravit Space Biol 22:21–33

    Google Scholar 

  • John SP, Hasenstein KH (2011) Effects of mechanostimulation on gravitropism and signal persistence in flax roots. Plant Signal Behav 6:1365–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauss H (1989) Fluorometric measurements of callose and other 1,3-β-glucans. In: Linskens H, Jackson J (eds) Plant Fibres. Springer-Verlag, Berlin, pp 127–137

    Chapter  Google Scholar 

  • Li S, Bashline L, Lei L, Gu Y (2014) Cellulose synthesis and its regulation. The Arabidopsis Book. Am Soc Plant Biol. doi: 10.1199/tab.0169

  • Lopez D, Tocquard K, Venisse J-S, Legué V, Roeckel-Drevet P (2014) Gravity sensing, a largely misunderstood trigger of plant orientated growth. Front Plant Sci 5. doi: 10.3389/fpls.2014.00610

  • Ma Z, Hasenstein KH (2006) The onset of gravisensitivity in the embryonic root of flax. Plant Physiol 140:159–166

    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 

  • Meloche CG, Knox JP, Vaughn KC (2007) A cortical band of gelatinous fibers causes the coiling of redvine tendrils: a model based upon cytochemical and immunocytochemical studies. Planta 225:485–498

    Article  CAS  PubMed  Google Scholar 

  • Meroz Y, Bastein R (2014) Stochastic Processes in Phototropism and Gravitropism. Front Plant Sci. doi:10.3389/fpls.2014.00674

  • Mikshina PV, Petrova AA, Faizullin DA, Zuev YF, Gorshkova TA (2015) Tissue-specific rhamnogalacturonan I forms the gel with hyperelastic properties. Biochem Mosc 80:915–924

    Article  CAS  Google Scholar 

  • Moulia B, Fournier M (2009) The power and control of gravitropic movements in plants: a biomechanical and systems biology view. J Exp Bot 60:461–486

    Article  CAS  PubMed  Google Scholar 

  • Nishikubo N, Awano T, Banasiak A, Bourquin V, Ibatullin F, Fundad R, Brumer H, Teeri TT, Hayashi T, Sundberg B, Mellerowicz EJ (2007) Xyloglucan endo-transglycosylase (XET) functions in gelatinous layers of tension wood fibers in Poplar—a glimpse into the mechanism the balancing act trees. Plant Cell Physiol 48:843–855

    Article  CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005) More than a leak sealant. The mechanical properties of callose in pollen tubes. Am J Plant Physiol 137:274–286

    Article  CAS  Google Scholar 

  • Patten AM, Jourdes M, Brown EE, Laborie M-P, Davin LB, Lewis NG (2007) Reaction tissue formation stem tensile modulus properties in wild-type and p-coumarate-3-hydroxylase downregulated lines of alfalfa, Medicago sativa (Fabaceae). Am J Bot 94:912–925

    Article  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J Cell Biol 17:208–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roach MJ, Deyholos MK (2007) Microarray analysis flax (Linum usitatissimum L.) stems identifies transcripts enriched in fibre-bearing phloem tissues. Mol Gen Genomics 278:149–165

    Article  CAS  Google Scholar 

  • Roach MJ, Mokshina NY, Snegireva AV, Badhan A, Hobson N, Deyholos MK, Gorshkova TA (2011) Development of cellulosic secondary walls in flax fibers requires β-galactosidase. Plant Physiol 156:1351–1363

    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 gelatinous secondary cell wall. Protoplasma 233:269–273

    Article  PubMed  Google Scholar 

  • Schreiber N, Gierlinger N, Putz N, Fratzl P, Neinhuis C, Burgert I (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 

  • Telewski FW (2006) A unified hypothesis of mechanoperception in plants. Am J Bot 93:1466–1476

    Article  PubMed  Google Scholar 

  • Toyota M, Gilroy S (2013) Gravitropism and mechanical signaling in plants. Am J Bot 100:111–125

    Article  CAS  PubMed  Google Scholar 

  • Wyatt SE, Sederoff R, Flaishman MA, Lev-Yadun S (2010) Arabidopsis thaliana a model for gelatinous fiber formation. Russ J Plant Physiol 57:384–388

    Article  Google Scholar 

Download references

Acknowledgments

The work was partially supported by Russian Foundation for Basic Research (grant # 15-04-05721).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nadezda N. Ibragimova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Alexander Schulz

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ibragimova, N.N., Ageeva, M.V. & Gorshkova, T.A. Development of gravitropic response: unusual behavior of flax phloem G-fibers. Protoplasma 254, 749–762 (2017). https://doi.org/10.1007/s00709-016-0985-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-016-0985-8

Keywords

Navigation