Abstract
Flax (Linum usitatissimum L.) phloem fibers elongate considerably during their development and intrude between existing cells. We questioned whether fiber elongation is caused by cell tip growth or intercalary growth. Cells with tip growth are characterized by having two specific zones of cytoplasm in the cell tip, one with vesicles and no large organelles at the very tip and one with various organelles amongst others longitudinally arranged cortical microtubules in the subapex. Such zones were not observed in elongating flax fibers. Instead, organelles moved into the very tip region, and cortical microtubules showed transversal and helical configurations as known for cells growing in intercalary way. In addition, pulse-chase experiments with Calcofluor White resulted in a spotted fluorescence in the cell wall all over the length of the fiber. Therefore, it is concluded that fiber elongation is not achieved by tip growth but by intercalary growth. The intrusively growing fiber is a coenocytic cell that has no plasmodesmata, making the fibers a symplastically isolated domain within the stem.
Similar content being viewed by others
Abbreviations
- CFW :
-
Calcofluor White
- CLSM :
-
Confocal laser scanning microscope
- GA :
-
Gluraraldehyde
- ESM :
-
Electronic supplementary material
- HAH :
-
Hydroxyltetra-ammoniumchloride
- Mes :
-
2-(N-morpholino)ethanesulphonic acid
- MSB :
-
Microtubule stabilizing buffer
- MT(s) :
-
Microtubule(s)
- PBS :
-
Phosphate buffered saline
- PFA :
-
Paraformaldehyde
- Pipes :
-
Piperazine-N,N′-bis(2-ethanesulfonic acid)
- RT :
-
Room temperature
- SP :
-
Snap point
References
de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G, Gheysen G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26 http://dx.doi.org/10.1111/j.1365-313X.2004.02019.x
Anderson DB (1927) A microchemical study of the structure and development of flax fibers. Amer J Bot 14 (1):187–211
Basra AS (ed) (1999) Cotton fibers: developmental biology, quality improvement, and textile processing. Food Products Press, Binghamton, p 387
Bichet A, Desnos T, Turner S, Grandjean O, Höfte H (2001) BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J 25:137–148 http://dx.doi.org/10.1046/j.1365-313x.2001.00946.x
Esau K (1943) Vascular differentiation in the vegetative shoot of Linum. III. The origin of bast fibers. Amer J Bot 30:579–586
Esau K (1977) Anatomy of seed plants. Wiley, New York
Fahn A (1990) Plant anatomy. Pergamon Press, Oxford, p 587
Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245 http://dx.doi.org/10.1046/j.1365-2818.2000.00702.x
Gorshkova TA, Ageeva MV, Sal’nikov VV, Pavlencheva NV, Snegireva AV, Chernova TE, Chemikosova SB (2003b) Stages of bast fiber formation in Linum usitatissimum L. Bot J (Russian) 12:1–11
Gorshkova TA, Sal’nikov VV, Chemikosova SB, Ageeva MV, Pavlencheva NV, van Dam JEG (2003a) The snap point: a transition point in Linum usitatissimum bast fiber development. Ind Crops and Prod 18:213–221 http://dx.doi.org/10.1016/S0926-6690(03)00043-8
Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NCA, Grierson CS, Dogterom M, Emons AMC (2002) Positioning of nuclei in Arabidopsis root hairs: an actin regulated process of tip growth. Plant Cell 14:2941–2955 http://dx.doi.org/10.1105/tpc.005892
Ketelaar T, de Ruijter NCA, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292 (Published online December 19, 2002; http://dx.doi.org/10.1105/tpc.007039
Lev-Yadun S (2001) Intrusive growth—the plant analog of dendrite and axon growth in animals. New Phytologist. 150: 508–512 http://dx.doi.org/10.1046/j.1469-8137.2001.00143.x
Lloyd C (1999) How I learned to love carrots: the role of the cytoskeleton in shaping plant cells. Bioessays, 21: 1061–1068 http://dx.doi.org/10.1002/(SICI)1521-1878(199912)22:1<1061::AID-BIES12>3.0.CO;2-2
McDougall GJ, Morrison IM, Steward D, Weyers JDB, Hillman JR (1993) Plant fibers: botany, chemistry and processing for industrial use. J Sci Food Agric 62:1–20
Miller DD, Leferink -ten Klooster HB, Emons AE (2000) Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hais. MPMI 13:1385–1390
Sieberer BJ, Timmers ACJ, Lhuissier FGP, Emons AMC (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiology 130:977–988 http://dx.doi.org/10.1104/pp.004267
Tiwari SC, Wilkins TA (1995) Cotton (Gossipium hirsutum) seed trichomes expand via diffuse growing mechanism. Can J Bot 73:746–757
Van Bruaene N, Joss G, van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136:3905–3919 http://dx.doi.org/10.1104/pp.103.031591
Van Lammeren AAM (1986) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immunofluorescence study. Protoplasma 146:18–27
Wasteneys G O (2000) The cytoskeleton and growth polarity. Curr Opin Plant Biol 3:503–511 http://dx.doi.org/10.1016/S1369-5266(00)00120-5
Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Ann Rev Plant Biol 54:691–722 http://dx.doi.org/10.1146/annurev.arplant.54.031902.134818
Acknowledgements
This work was supported by the program Molecular and Cellular Biology of the Russian Academy of Sciences (MCB RAS), by grants 03-04-96223 and 03-3.10-232 of the Russian Foundation of Basic Research (RFBR) -Tatarstan scientific program, and by fellowships of The Dutch Ministry of Agriculture, Nature Management and Fisheries to AMV and PB. We thank Dr. L.E. Muravnik (Botanical Institute, St. Petersburg) for the help in statistical evaluation of electron microscopy data.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ageeva, M.V., Petrovská, B., Kieft, H. et al. Intrusive growth of flax phloem fibers is of intercalary type. Planta 222, 565–574 (2005). https://doi.org/10.1007/s00425-005-1536-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-005-1536-2