Abstract
Using light and electron microscopy, the early stages of root hair initiation were investigated under control conditions and in a situation where F-actin polymerization was effectively inhibited by latrunculin B. Trichoblasts in their early stage of bulge formation possessed large vacuole traversed by cytoplasmic strands and enclosed within a narrow peripheral layer of cytoplasm. The nucleus was settled at the inner periclinal cell wall, typically opposite the site of bulge formation. Within the bulging area, dense cytoplasm and numerous ER elements, and other organelles were accumulated, together with pleiomorphic membrane-bound structures, the identity and nature of which will require further studies. These unusual structures, which were associated with the outer cell wall, contained material similar to that of the cell wall. Similar cell wall-like bodies were observed also in the cytoplasm and sometimes within vacuoles. The possible role of these novel organelles of plant cells in cell wall thinning/degradation or in the turgor pressure maintenance are discussed. Latrunculin B treatment allowed bulge formation but prevented the switch from the slow and diffuse expansion of bulge into the rapid tip-growth characteristic of the emerging root hair. Moreover, the cytoplasm of the bulging domain became extensively vacuolated and lacked abundant ER elements and other organelles including the membrane-bound structures. These results indicate important roles of F-actin in the switch from diffuse to highly polarized tip growth.
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Baluška F, Barlow P W and Volkmann D 2000a Actin and myosin VIII in developing root apex cells. In Actin: a Dynamic Framework for Multiple Plant Cell Functions. Eds. C J Staiger, F Baluška, D Volkmann and P W Barlow. pp. 457–476. Kluwer Academic Publishers, Dordrecht.
Baluška F, Salaj J, Mathur J, Braun M, Jasper F, Šamaj J, Chua N-H, Barlow P W and Volkmann D 2000b Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev. Biol. 227, 618–632.
Baluška F, Volkmann D and Barlow P W 2000c Actin-based domains of the “ell periphery complex” and their associations with polarized "cell bodies" in higher plants. Plant Biol. 2, 253–267.
Baluška F, Ovečka M and Hirt H 2000d Salt stress-and cell cycle phase-dependent changes in expression and subcellular localisation of the alfalfa mitogen-activated protein kinase SIMK. Protoplasma 212, 262–267.
Baluška F, Jásik J, Edelmann H G, Salajová T and Volkmann D 2001 Latrunculin B-induced plant dwarfism: plant cell elongation is actin-dependent. Dev. Biol. 231, 113–124.
Baluška F and Volkmann D 2002 Actin-driven polar growth of plant cells. Trends Cell Biol. 12, 14.
Baumberger N, Ringli C and Keller B 2001 The chimeric leucinerich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev. 15, 1128–1139.
Bibikova T N, Jacob T, Dahse I and Gilroy S 1998 Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125, 2925–2934.
Braun M, Baluška F, von Witsch M and Menzel D 1999 Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209, 435–443.
Bucher M, Schroeer B, Willmitzer L and Riesmeier J W 1997 Two genes encoding extensin-like proteins are predominantly expressed in tomato root hair cells. Plant Mol. Biol. 35, 497–508. Čiamporová M and Mistrík I 1993 The ultrastructural response of root cells to stressful conditions. Environ. Exp. Bot. 33, 11–26.
De Ruijter N C A, Rook M B, Bisseling T and Emons A M C 1998 Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J. 13, 341–350.
Dolan L 2001 How and where to build a root hair. Curr. Opin. Plant Biol. 4, 550–554.
Emons A M C and de Ruijter N 2000 Actin: a target of signal transduction in root hairs. In Actin: a Dynamic Framework for Multiple Plant Cell Functions. Eds. C J Staiger, F Baluška, D. Volkmann and P W Barlow. pp. 373–390. Kluwer Academic Publishers, Dordrecht.
Fårhaeus G 1957 The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen.Microbiol. 16, 374–381.
Favery B, Ryan E, Foreman J, Linstead P, Boundonck K, Steer M, Shaw P and Dolan L 2001 KOJAK encodes a cellulose-synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev. 15, 79–89.
Galway ME, Lane D C and Schiefelbein JW 1998 Defective control of growth rate and cell diameter in tip-growing root hairs of the rhd4 mutant of Arabidopsis thaliana. Can. J. Bot. 77, 494–507.
Geitmann A and Emons A M C 2000 The cytoskeleton in plant and fungal cell tip growth. J. Microsc. 198, 218–245.
Jiang C-J, Weeds A G and Hussey PJ 1997 The maize actindepolymerizing factor, ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actin. Plant J. 12, 1035–1043.
Kost, B and Chua N-H 2002 The plant cytoskeleton: vacuoles and cell walls make the difference. Cell 108, 9–12.
Kost B, Mathur J and Chua N-H 1999 Cytoskeleton in plant development. Curr. Opin. Plant Biol. 2, 462–470.
Mathur J and Hülskamp M 2001 How to grow and where to grow. Curr. Biol. 11, R402–R404.
Miller D D, De Ruijter N A, Bisseling T and Emons A M C 1999 The role of actin in root hair morphogenesis. Studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J. 17, 141–154.
Miller D D, Leferink ten Klooster H B and Emons A M C 2000 Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol. Plant-Microbe Interact. 13, 1385–1390.
Molendijk A J, Bischoff F, Rajendrakumar C S, Friml J, Braun M, Gilroy S and Palme K 2001 Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 20, 2779–2788.
Nishizawa N K, Tainaka H, Okubo A, Ishida N and Mori S 1989 Desiccation-induced heterophagy in plant root cells. In Structural and Functional Responses to Environmental Stresses:Water Shortage. Eds. K H Krebs, H Richter and T M Hinckley. pp. 99–111. SPB Academic Publishing, The Hague.
Ovečka M, Baluška F, Nadubinská M and Volkmann D 2000 Actomyosin and exocytosis inhibitors alter root hair morphology in Poa annua L. Biologia 55, 105–114.
Ringli C, Baumberger N, Diet A, Frey B and Keller B 2002 ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol. 129, 1464–1472.
Ryan E, Steer M and Dolan L 2001 Cell biology and genetics of root hair formation in Arabidopsis thaliana. Protoplasma 215, 140–149.
Šamaj J, Braun M, Baluška F, Ensikat H-J, Tsumuraya Y and Volkmann D 1999 Specific localization of arabinogalactan-protein epitopes at the surface of maize root hairs. Plant Cell Physiol. 40, 874–883.
Šamaj J, Ovečka M, Hlavačka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluška F and Hirt H 2002 Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growth. EMBO J. 21, 3296–3306.
Schiefelbein JW 2000 Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124, 1525–1531.
Schiefelbein J W and Sommerville C 1990 Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2, 235–243.
Slaninová I, Šesták S, Svoboda A and Farkaš V 2000 Cell wall and cytoskeleton reorganization as the response to hyperosmotic shock in Saccharomyces cerevisieae. Arch. Microbiol. 173, 245–252.
Staiger C J, Baluška F, Volkmann D and Barlow PW 2000 Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic Publishers, Dordrecht, pp. 663.
Vissenberg K, Fry S C and Verbelen J-P 2001 Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol. 127, 1125–1135.
Volkmann D and Baluška F 1999 Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc. Res. Tech. 47, 135–154.
Volkmann D and Peters P 1995 Structural basis of root hair formation: Early development of trichoblasts and atrichoblasts. In Structure and Function of Roots. Eds. F Baluška, M Čiamporová, O Gašparíková and P W Barlow. pp. 61–67. Kluwer Academic Publishers, Dordrecht.
Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M and Van Lijsebettens M 2001 Atclsd3, a cellulose-synthaselike gene important for root hair growth in Arabidopsis. Plant Physiol. 126, 575–586.
Yokota E, Imamichi N, Tominanga M and Shimmen T 2000 Actin cytoskeleton is responsible for the change of cytoplasmic organization in root hair cells induced by a protein phosphatase inhibitor, calyculin A. Protoplasma 213, 184–193.
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iamporová, M., Dekánková, K., Haná ková, Z. et al. Structural aspects of bulge formation during root hair initiation. Plant and Soil 255, 1–7 (2003). https://doi.org/10.1023/A:1026151000063
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DOI: https://doi.org/10.1023/A:1026151000063