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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing

Przemysław Wojtaszek A B D , Anna Anielska-Mazur C , Halina Gabryś C , František Baluška A and Dieter Volkmann A
+ Author Affiliations
- Author Affiliations

A Institute of Cellular and Molecular Botany, Rheinische Friedrich-Wilhelms-Universität Bonn, Kirschallee 1, 53115 Bonn, Germany.

B Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University, Fredry 10, 61-701 Poznań, and Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704 Poznań, Poland.

C Department of Plant Physiology and Biochemistry, Faculty of Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland.

D Corresponding author. Email: przemow@ibch.poznan.pl

Functional Plant Biology 32(8) 721-736 https://doi.org/10.1071/FP05004
Submitted: 30 December 2004  Accepted: 22 April 2005   Published: 3 August 2005

Abstract

The existence of a cell wall–plasma membrane–cytoskeleton (WMC) continuum in plants has long been postulated. However, the individual molecules building such a continuum are still largely unknown. We test here the hypothesis that the integrin-based multiprotein complexes of animal cells have been replaced in plants with more dynamic entities. Using an experimental approach based on protoplast digestion mixtures, and utilising specific antibodies against Arabidopsis ATM1 myosin, we reveal possible roles played by plant-specific unconventional myosin VIII in the functioning of WMC continuum. We demonstrate rapid relocation (less than 5 min) of myosin VIII to statolith surfaces in maize root-cap cells, which is accompanied by the reorganisation of actin cytoskeleton. Upon prolonged stimulation, myosin VIII is also recruited to plasmodesmata and pit-fields of plasmolysing root cap statocytes. The osmotic stimulus is the major factor inducing relocation, but the cell wall–cytoskeleton interactions also play an important role. In addition, we demonstrate the tight association of myosin VIII with the surfaces of chloroplasts, and provide an indication for the differences in the mechanisms of plastid movement in roots and leaves of plants. Overall, our data provide evidence for the active involvement of actomyosin complexes, rooted in the WMC continuum, in the cellular volume control and maintenance of spatial relationships between cellular compartments.

Keywords: actin, cell wall–cytoskeleton interactions, myosin VIII (unconventional), organelle movement, osmosensing, plastids, root cap, statolith.


Acknowledgments

This work was supported by a fellowship to PW from Alexander von Humboldt Foundation (Bonn, Germany). We thank Jerzy Dobrucki (Jagiellonian University, Poland) for the access to the confocal microscope. We thank Chris Staiger (Purdue University, USA) for providing us with antibodies against maize pollen actin. The financial provision from the Deutches Zentrum für Luft- und Raumfahrt, Köln, Germany (DV) and from European Commission (5th Framework Program, Centre of Excellence grants ICA1–1999–70105 and ICA-CT-2000–70012 to Faculty of Biotechnology, Jagiellonian University) is also gratefully acknowledged.


References


Anderson CM, Wagner TA, Perret M, He Z-H, He D, Kohorn BD (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Molecular Biology 47, 197–206.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aon MA, Cortassa S, Gomez Casati DF, Iglesias AA (1999) Effects of stress on cellular infrastructure and metabolic organization in plant cells. International Review of Cytology 194, 239–273. open url image1

Aronsson H, Jarvis P (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Letters 529, 215–220.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baluška F, Hasenstein KH (1997) Root cytoskeleton: its role in perception of and response to gravity. Planta 203, S69–S78.
PubMed |
open url image1

Baluška F, Parker JS, Barlow PW (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). Journal of Cell Science 103, 191–200. open url image1

Baluška F, Busti E, Dolfini S, Gavazzi G, Volkmann D (2001a) Liliputian mutant of maize lacks cell elongation and shows defects in organization of actin cytoskeleton. Developmental Biology 236, 478–491.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baluška F, Cvrcková F, Kendrick-Jones J, Volkmann D (2001b) Sink plasmodesmata as gateways for phloem unloading: myosin VIII and calreticulin as molecular determinants of sink strength. Plant Physiology 126, 39–47.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003a) Cytoskeleton–plasma membrane–cell wall continuum in plants. Emerging links revisited. Plant Physiology 133, 482–491.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baluška F, Wojtaszek P, Volkmann D (2003b) The architecture of polarized cell growth: the unique status of elongating plant cells. BioEssays 25, 569–576.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baluška F, Šamaj J, Hlavačka A, Kendrick-Jones J, Volkmann D (2004) Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices. Journal of Experimental Botany 55, 463–473.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bezanilla M, Horton AC, Sevener HC, Quatrano RS (2003) Phylogenetic analysis of new plant myosin sequences. Journal of Molecular Evolution 57, 229–239.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60, 357–364.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Braun M (2002) Gravity perception requires statoliths settled on specific plasma membrane areas in characean rhizoids and protonemata. Protoplasma 219, 150–159.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brownlee C (2002) Role of the extracellular matrix in cell–cell signaling: paracrine paradigms. Current Opinion in Plant Biology 5, 396–401.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brownlee C, Goddard H, Hetherington AM, Peake L-A (1999) Specificity and integration of responses: Ca2+ as a signal in polarity and osmotic regulation. Journal of Experimental Botany 50, 1001–1011.
Crossref | GoogleScholarGoogle Scholar | open url image1

Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Molecular Biology of the Cell 12, 323–337.
PubMed |
open url image1

Centis-Aubay S, Gasset G, Mazars C, Ranjeva R, Graziana A (2003) Changes in gravitational forces induce modifications of gene expression in A. thaliana seedlings. Planta 218, 179–185.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cheung AY, Wu H-M (2004) Overexpression of an Arabidopsis forming stimulates supernumerary actin cable formation from pollen tube cell membrane. The Plant Cell 16, 257–269.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chinchilla D, Merchan F, Megias M, Kondorosi A, Sousa C, Crespi M (2003) Ankyrin protein kinases: a novel type of plant kinase gene whose expression is induced by osmotic stress in alfalfa. Plant Molecular Biology 51, 555–566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ding JP, Pickard BG (1993) Mechanosensory calcium-selective cation channels in epidermal cells. The Plant Journal 3, 83–110.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dixon KP, Xu J-R, Smirnoff N, Talbot NJ (1999) Independent signalling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea.  The Plant Cell 11, 2045–2058.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Felix G, Regenass M, Boller T (2000) Sensing of osmotic pressure changes in tomato cells. Plant Physiology 124, 1169–1179.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Forgacs G (1995) On the possible role of cytoskeletal filamentous networks in intracellular signaling: an approach based on percolation. Journal of Cell Science 108, 2131–2143.
PubMed |
open url image1

Hamill OP, Martinac B (2001) Molecular basis of mechanotransduction in living cells. Physiological Reviews 81, 685–740.
PubMed |
open url image1

Hayashi T, Takagi S (2003) Ca2+-dependent cessation of cytoplasmic streaming induced by hypertonic treatment in Vallisneria mesophyll cells: possible role of cell wall–plasma membrane adhesion. Plant and Cell Physiology 44, 1027–1036.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hashimoto K, Igarashi H, Mano S, Nishimura M, Teruo S, Yokota E (2005) Peroxisomal localization of a myosin XI isoform in Arabidopsis thaliana. Plant and Cell Physiology 46, 782–789.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hejnowicz Z, Rusin A, Rusin T (2000) Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. Journal of Plant Growth Regulation 19, 31–44.
PubMed |
open url image1

Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiology and Molecular Biology Reviews 66, 300–372.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Holweg C, Nick P (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proceedings of the National Academy of USA 101, 10488–10493.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hwang I, Chen H-C, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiology 129, 500–515.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ingber DE (2003) Tensegrity II. How structural networks influence cellular information processing networks. Journal of Cell Science 116, 1397–1408.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jedd G, Chua N-H (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant and Cell Physiology 43, 384–392.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kandasamy MK, Meagher RB (1999) Actin organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motility and the Cytoskeleton 44, 110–118.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Katz B-Z, Zamir E, Bershadsky A, Kam Z, Yamada KM, Geiger B (2000) Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Molecular Biology of the Cell 11, 1047–1060.
PubMed |
open url image1

Kern VD, Smith JD, Schwuchow JM, Sack FD (2001) Amyloplasts that sediment in protonemata of the moss Ceratodon purpureus are nonrandomly distributed in microgravity. Plant Physiology 125, 2085–2094.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kobayashi Y, Hakuno H (2003) Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217, 340–345.
PubMed |
open url image1

Kobayashi Y, Yamada M, Kobayashi I, Kunoh H (1997) Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant and Cell Physiology 38, 725–733. open url image1

Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminium activates citrate-permeable anion channel in the aluminium-sensitive zone of the maize root apex. A comparison between an aluminium-sensitive and an aluminium-insensitive cultivar. Plant Physiology 126, 397–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Komis G, Apostolakos P, Galatis B (2002) Hyperosmotic stress-induced actin filament reorganization in leaf cells of Chlorophyton comosum.  Journal of Experimental Botany 53, 1699–1710.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Komis G, Apostolakos P, Galatis B (2003) Actomyosin is involved in the plasmolytic cycle: gliding movement of the deplasmolyzing protoplast. Protoplasma 221, 245–256.
PubMed |
open url image1

Lang I, Barton DA, Overall RL (2004) Membrane-wall attachments in plasmolysed plant cells. Protoplasma 224, 231–243.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lang-Pauluzzi I, Gunning BES (2000) A plasmolytic cycle: the fate of cytoskeletal elements. Protoplasma 212, 174–185.
Crossref | GoogleScholarGoogle Scholar | open url image1

Liebe S, Menzel D (1995) Actomyosin-based motility of endoplasmic reticulum and chloroplasts in Vallisneria mesophyll cells. Biology of the Cell 85, 207–222.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu L, Zhou J, Pesacreta TC (2001) Maize myosins: diversity, localization, and function. Cell Motility and the Cytoskeleton 48, 130–148.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lord EM, Mollet J-C (2002) Plant cell adhesion: a bioassay facilitates discovery of the first pectin biosynthetic gene. Proceedings of the National Academy of Sciences USA 99, 15843–15845.
Crossref | GoogleScholarGoogle Scholar | open url image1

Malec P, Rinaldi RA, Gabryś H (1996) Light-induced chloroplast movements in Lemna trisulca. Identification of the motile system. Plant Science 120, 127–137.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marshall JG, Dumbroff EB (1999) Turgor regulation via cell wall adjustment in white spruce. Plant Physiology 119, 313–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mathur J, Mathur N, Hülskamp M (2002) Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiology 128, 1031–1045.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Menczel L, Nagy F, Kiss Z, Maliga P (1981) Streptomycin resistant and sensitive somatic hybrids of N. tabacum + N. knightiana: correlation of resistance to N. tabacum plastids. Theoretical and Applied Genetics 59, 191–195.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mikołajczyk M, Awotunde OS, Muszyńska G, Klessig DF, Dobrowolska G (2000) Osmotic stress induced rapid activation of a salicylic acid-induced protein kinase an a homolog of protein kinase ASK1 in tobacco cells. The Plant Cell 12, 165–178.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moseyko N, Zhu T, Chang H-S, Wang X, Feldman LJ (2002) Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarray. Plant Physiology 130, 720–728.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nakagawa N, Sakurai N (2001) Cell wall integrity controls expression of endoxyloglucan transferase in tobacco BY2 cells. Plant and Cell Physiology 42, 240–244.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanagae T, Niwa Y, Kadota A, Wada M (2003) CHLOROPLAST UNUSUAL POSITIONING1 is essential for proper chloroplast positioning. The Plant Cell 15, 2805–2815.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytologist 126, 571–591. open url image1

Oparka KJ, Prior DAM (1992) Direct evidence for pressure-generated closure of plasmodesmata. The Plant Journal 2( ), 741–750. open url image1

Paul AL, Schuerger AC, Popp MP, Richards JT, Manak MS, Ferl RJ (2004) Hypobaric biology: Arabidopsis gene expression at low atmospheric pressure. Plant Physiology 134, 215–223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peters WS, Hagemann W, Tomos DA (2000) What makes plants different? Principles of extracellular matrix function in ‘soft’ plant tissues. Comparative Biochemistry and Physiology. Part A 125, 151–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reddy ASN, Day IS (2001) Analysis of myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biology 2, 0024.1–0024.17.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reichelt S, Knight AE, Hodge TP, Baluška F, Šamaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. The Plant Journal 19, 555–569.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sack FD (1991) Plant gravity sensing. International Review of Cytology 127, 193–252.
PubMed |
open url image1

Sato Y, Wada M, Kadota A (2001) Choice of tracks, microtubules and / or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. Journal of Cell Science 114, 269–279.
PubMed |
open url image1

Sheahan MB, Rose RJ, McCurdy DW (2004) Organelle inheritance in plant cell division: the actin cytoskeleton is required for unbiased inheritance of chloroplasts, mitochondria and endoplasmic reticulum in dividing protoplasts. The Plant Journal 37, 379–390.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shepherd VA, Beilby MJ, Shimmen T (2002) Mechanosensory ion channels in charophyte cells: the response to touch and salinity stress. European Biophysics Journal 31, 341–355.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sivaguru M, Ezaki B, Osawa H, Baluška F, Volkmann D, Matsumoto H (2003) Aluminum-induced gene expression and protein localization of cell wall-associated receptor kinase in Arabidopsis thaliana.  Plant Physiology 132, 2256–2266.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Soga K, Wakabayashi K, Kamisaka S, Hoson T (2005) Mechanoreceptors rather than sedimentable amyloplasts perceive the gravity signal in hypergravity-induced inhibition of root growth in azuki bean. Functional Plant Biology 32, 175–179.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Staves MP (1997) Cytoplasmic streaming and gravity sensing in Chara internodal cells. Planta 203, S79–S84.
PubMed |
open url image1

Swartz MA, Rschumperlin DJ, Kamm RD, Drazen JM (2001) Mechanical stress is communicated between different cell types to elicit matrix remodeling. Proceedings of the National Academy of Sciences USA 98, 6180–6185.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van Gestel K, Kohler RH, Verbelen J-P (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. Journal of Experimental Botany 53, 659–667.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Volkmann, D ,  and  Baluška, F (2000). Actin cytoskeleton related to gravisensing in higher plants. In ‘Actin: a dynamic framework for multiple plant cell functions’. pp. 557–571. (Kluwer Academic Publishers: Dordrecht)

Wang Z, Pesacreta TC (2004) A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone TCP-1α in maize. Cell Motility and the Cytoskeleton 57, 218–232.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. Journal of Cell Science 101, 611–623.
PubMed |
open url image1

Wojtaszek P (2000) Genes and plant cell walls: a difficult relationship. Biological Reviews of the Cambridge Philosophical Society 75, 437–475.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wojtaszek P (2001) Organismal view of a plant and a plant cell. Acta Biochimica Polonica 48, 443–451.
PubMed |
open url image1

Wyatt SE, Carpita NC (1993) The plant cytoskeleton–cell wall continuum. Trends in Cell Biology 3, 413–417.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yoder TL, Zheng H-Q, Todd P, Staehelin LA (2001) Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus in roots. Plant Physiology 125, 1045–1060.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yokota E (2000) Identification and characterization of higher plant myosins responsible for cytoplasmic streaming. Journal of Plant Research 113, 511–519. open url image1

Zhang H, Berg JS, Li Z, Wang Y, Lång P, Sousa AD, Bhaskar A, Cheney RE, Strömblad S (2004) Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nature Cell Biology 6, 523–531.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao H-P, Liu A-X, Ren D-T, Liu G-Q, Yan L-F (1999) Identification of myosin on the surface of wheat mitochondria. Acta Botanica Sinica 41, 1303–1306. open url image1

Zonia L, Munnik T (2004) Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiology 134, 813–823.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1