Short-Term Boron Deprivation Induces Increased Levels of Cytoskeletal Proteins in Arabidopsis Roots

Q. Yu; R. Wingender; M. Schulz; F. Baluška; H. E. Goldbach

doi:10.1055/s-2001-16452

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2001; 3(4): 335-340
DOI: 10.1055/s-2001-16452

Original Paper

Georg Thieme Verlag Stuttgart ·New York

Short-Term Boron Deprivation Induces Increased Levels of Cytoskeletal Proteins in Arabidopsis Roots

Q. Yu ^1,4 , R. Wingender ² , M. Schulz ² , F. Baluška ³ , H. E. Goldbach ¹

¹ Agricultural Chemistry Institute, University of Bonn, Bonn, Germany
² Agricultural Botany, University of Bonn, Bonn, Germany
³ Botany Institute, University of Bonn, Bonn, Germany
⁴ College of Biotechnology, South China Agricultural University, Guangzhou, 510642 China

Abstract

Although boron is known to be an essential element for the growth of all higher plants, the links between primary responses to boron deprivation and the expression of visual symptoms are yet unknown. Western blots with anti-actin and anti-tubulin antibodies revealed an increase of both proteins upon 20 - 40 min of boron deprivation in roots of hydroponically grown Arabidopsis thaliana. Moreover, actin depolymerizing factor and myosin VIII showed a less pronounced but similiar response to boron deficiency. In contrast, no increase in higher molecular mass ubiquitin was observed, indicating an absence of intensive protein degradation during the experimental time span. This is the first report of cytoskeletal responses of plants to short-term boron removal. Rapid elevation of cytoskeletal proteins after boron deprivation is discussed in relation to the cell wall-plasma membrane-cytoskeleton continuum.

Key words

Actin - ADF (actin depolymerizing factor) - Arabidopsis - boron deprivation - myosin - roots - tubulin - ubiquitin

Full Text

References

01 Baluška, F.,, Volkmann, D.,, and Barlow, P. W.. (2000); Actin-based domains of the “cell periphery complex” and their associations with polarized “cell bodies” in higher plants. Plant Biol.. 2 253-267
02 Baluška, F.,, Jasik, J.,, Edelmann, H. G.,, Salajová, T.,, and Volkmann, D.. (2001); Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin dependent. Dev. Biol.. 231 113-124
03 Barlow, P. W., and Baluška, F.. (2000); Cytoskeletal perspectives on root growth and morphogenesis. Ann. Rev. Plant Physiol. Plant Mol. Biol.. 51 289-322
04 Ben-Ze'ev, A.,, Farmer, S. R.,, and Penman, S.. (1979); Mechanisms of regulating tubulin synthesis in cultured mammalian cells. Cell. 17 310-325
05 Bershadsky, A. D.,, Gluck, U.,, Denisenko, O. N.,, Sklyarova, T. V.,, Spector, I.,, and Ben-Ze'ev, A.. (1995); The state of actin assembly regulates actin and vinculin expression by a feedback loop. J. Cell Sci.. 108 1183-1193
06 Blancaflor, E. B.,, Jones, D. L.,, and Gilroy, S.. (1998); Alterations in the cytoskeleton accompany aluminum induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol.. 118 159-172
07 Burke, T. J.,, Callis, J.,, and Vierstra, R. D.. (1988); Characterization of a polyubiquitin gene from Arabidopsis thaliana. . Mol. Gen. Genet.. 213 435-443
08 Cappelletti, G.,, Maggioni, M. G,, Carnevali, M. D. C.,, Bonasoro, F.,, and Maci, R.. (1996); Dynamic changes in the state of actin polymerization in human alveolar cells exposed to the oxidant agent paraquat. Eur. J. Cell Biol.. 71 293-302
09 Cyr, R.. (1991); Calcium/calmodulin affects microtubule stability in lysed protoplasts. J. Cell Sci.. 100 311-317
10 Findeklee, P.,, Wimmer, M.,, and Goldbach, H. E.. (1997) Early effects of boron deficiency on physical cell wall parameters, hydraulic conductivity and plasmalemma-bound reductase activities in young C. pepo and V. faba roots. Boron in Soil and Plants, Proceedings. Bell, R. and Rerkasem, B., eds. Dordrecht, Netherlands; Kluwer Academic Publishers pp. 221-227
11 Fleischer, A.,, O'Neill, M. A.,, and Ehwald, R.. (1999); The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol.. 121 829-838
12 Goldbach, H. E.. (1997); A critical review on current hypotheses concerning the role of boron in higher plants: suggestions for further research and methodological requirements. J. Trace Micr. Techn.. 15 51-91
13 Goldbach, H. E.,, Wimmer, M. A.,, and Findeklee, P.. (2000); Discussion paper: Boron - how can the critical level be defined?. J. Plant Nutr. Soil Sci.. 163 115-121
14 Grabski, S.,, Arnoys, E.,, Busch, B.,, and Schindler, M.. (1998); Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol.. 116 279-290
15 Horst, W. J.,, Schmohl, N.,, Kollmeier, M.,, Baluška, F.,, and Sivaguru, M.. (1999); Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum?. Plant Soil. 215 163-174
16 Hunte, C.,, Traub, O.,, Schnabl, H.,, Willeck, K.,, and Schulz, M.. (1992); Immunological evidence of connexin-like plant proteins in the plasma membrane of Vicia faba L. Bot. Acta. 105 104-110
17 Hussey, P. J., and Gull, K.. (1985); Multiple isotypes of α- and β-tubulin in the plant Phaseolus vulgaris. . FEBS Lett.. 181 113-118
18 Janßen, M.,, Hunte, C.,, Schulz, M.,, and Schnabl, H.. (1996); Tissue specification and intracellular distribution of actin isoforms in Vicia faba L. Protoplasm. 191 158-163
19 Jones, D. L.,, Kochian, L. V.,, and Gilroy, S.. (1998); Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell cultures. Plant Physiol.. 116 81-89
20 Kampen van, J.,, Wettern, J.,, and Schulz, M.. (1996); The ubiquitin system in plants. Physiol. Plant. 97 618-624
21 Kerr, P. G., and Carter, J. V.. (1990); Tubulin isotypes in rye roots are altered during cold acclimation. Plant Physiol.. 93 83-88
22 Kobayashi, M.,, Matoh, T.,, and Azuma, J.-I.. (1996); Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol.. 110 1017-1020
23 Koyama, H.,, Toda, T.,, Kojima, H.,, and Hara, T.. (1995); Direct observation of root-elongation of Arabidopsis thaliana seedlings grown in hydroponic culture. Soil Sci. Plant Nutr.. 41 173-176
24 Lenoble, M. E.,, Blevins, D. G.,, Sharp, R. E.,, and Cumbie, B. G.. (1996); Prevention of aluminium toxicity with supplemental boron. 1. Maintenance of root elongation and cellular structure. Plant, Cell and Envir.. 19 1132-1142
25 Lyubimova, A.,, Bershadsky, A. D.,, and Ben-Ze'ev, A.. (1997); Autoregulation of actin synthesis responds to monomeric actin levels. J. Cell. Biochem.. 65 469-478
26 Matoh, T.. (1997); Boron in plant cell walls. Plant Soil. 193 59-70
27 Matoh, T.,, Takasaki, M.,, Takabe, K.,, and Kobayashi, M.. (1998); Immunocytochemistry of rhamnogalacturonan II in cell walls of higher plants. Plant Cell Biol.. 39 483-491
28 McDowell, J M.,, An, Y. Q.,, Huang, S.,, Mckinney, E. C.,, and Meagher, R. B.. (1996); The Arabidopsis ACT7 actin gene is expressed in rapidly developing tissues and responds to several external stimuli. Plant Physiol.. 111 699-711
29 McLean, B G.,, Huang, S.,, Mckinney, E. C.,, and Meagher, R. B.. (1990); Plant contains highly divergent actin isovariants. Cell Motil. Cytoskel.. 17 276-290
30 Miller, D.,, Hable, W.,, Gottwald, J.,, Ellard-Ivey, M.,, Demura, T.,, Lomax, T.,, and Carpita, N.. (1997); Connections: the hard wiring of the plant cell for perception, signaling, and response. Plant Cell. 9 2105-2117
31 Mizuno, K.,, Perkin, J.,, Sek, F.,, and Gunning, B. E. S.. (1985); Some biochemical properties of higher plant tubulins. Cell Biol. Int. Rep.. 9 5-12
32 Mühling, K. H.,, Wimmer, M.,, and Goldbach, H. E.. (1998); Apolastic and membrane-associated Ca²⁺ in leaves and roots as affected by boron deficiency. Physiol. Plant.. 102 179-184
33 Pérez, H.,, Sánchez, N.,, Vidali, L.,, Maunel Hernández, L.,, Lara, M.,, and Sánchez, F.. (1994); Actin isoforms in non-infected roots and symbiotic root nodules of Paseolus vulgaris L. Planta. 193 51-56
34 Reichelt, S., and Kendrick-Jones, J.. (2000) Myosins. Actin: a Dynamic Framework for Multiple Plant Cell Functions. Staiger, C. J., Baluška, F., Volkmann, D., and Barlow, P. W., eds. Kluwer Academic Publishers pp. 29-44
35 Reichelt, S.,, Knight, A. E.,, Hodge, T. P.,, Baluška, F.,, Šamaj, J.,, Volkmann, D.,, and Kendrick-Jones, J.. (1999); Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J.. 19 555-569
36 Reuner, K. H.,, Wiederhold, M.,, Schlegel, K.,, Just, I.,, and Katz, N.. (1995); Autoregulation of actin synthesis by physiological alterations of the G-actin level in hepatocytes. Euro. J. Clinical Chem. Clinical Biochem.. 33 569-574
37 Šamaj, J.,, Peters, M.,, Volkmann, D.,, and Baluška, F.. (2000); Effects of myosin ATPase inhibitor 2,3-butanedione 2-monoxime on distribution of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol.. 41 571-582
38 Schmohl, N., and Horst, W. J.. (2000); Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environm.. 23 735-742
39 Seagull, R. W.. (1989); The plant cytoskeleton. Cri. Rev. Plant Sci.. 8 131-167
40 Sivaguru, M.,, Baluška, F.,, Volkmann, D.,, Felle, H. H.,, and Horst, W. J.. (1999); Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol.. 119 1073-1082
41 Staiger, C. J.,, Gibbon, B. C.,, Kovar, D. R.,, and Zonia, L. E.. (1997); Profilin and actin-depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci.. 2 275-281
42 Volkmann, D., and Baluška, F.. (1999); The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc. Res. Tech.. 47 135-154
43 Wyatt, S. E., and Carpita, N. C.. (1993); The plant cytoskeleton-cell wall continuum. Trends Cell Biol.. 3 413-417

H. Goldbach

Institute of Agricultural Chemistry

Karlrobert-Kreiten-Straße 13
53115 Bonn
Germany

Email: h.goldbach@uni-bonn.de

Section Editor: H. Rennenberg