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

Early events in the signalling pathway for the activation of MAPKs in rice roots exposed to nickel

Po-Yu Chen A B , Tsai-Lien Huang A B and Hao-Jen Huang A C
+ Author Affiliations
- Author Affiliations

A Department of Life Sciences, National Cheng Kung University, No. 1 University Road, 701 Tainan, Taiwan, ROC.

B These authors contributed equally to this article.

C Corresponding author. Email: haojen@mail.ncku.edu.tw

Functional Plant Biology 34(11) 995-1001 https://doi.org/10.1071/FP07163
Submitted: 25 June 2007  Accepted: 19 July 2007   Published: 1 November 2007

Abstract

It is well known that small quantities of nickel (Ni) are essential for plant species, and higher concentrations of Ni retard plant growth. However, the molecular mechanisms responsible for the regulation of plant growth by Ni are not well understood. The aim of this study is to investigate the early signalling pathways activated by Ni on rice (Oryza sativa L.) root. We showed that Ni elicited a remarkable increase in myelin basic protein (MBP) kinase activities. By immunoblot and immunoprecipitation analyses, it is suggested that Ni-activated 40- and 42-kDa MBP kinases are mitogen-activated protein kinases (MAPKs). Pretreatment of rice roots with the antioxidant, glutathione (GSH), the phospholipase D (PLD) inhibitor, n-butanol, and the calmodulin and CDPK antagonist and W7 inhibited Ni-induced MAPK activation. These results suggest that various signalling components are involved in transduction of the Ni signal in rice roots.

Additional keywords: Ni, phosphorylation.


Acknowledgements

This work was supported by research grants from the National Science Council (NSC 95–2311-B-006–002; NSC 96–2311-B-006–001) and the Ministry of Education of the Republic of China (‘Landmark Project Grant’ for NCKU’s ‘Top-University Project’, B024).


References


Abo-El-Saad M, Wu R (1995) A rice membrane calcium-dependent protein kinase is induced by gibberellin. Plant Physiology 108, 787–793.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Agrawal GK, Iwahashi H, Rakwal R (2003) Rice MAPKs. Biochemical and Biophysical Research Communications 302, 171–180.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Allan AC, Maddumage R, Simons JL, Neill SO, Ferguson IB (2006) Heat-induced oxidative activity protects suspension-cultured plant cells from low temperature damage. Functional Plant Biology 33, 67–76.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baccouch S, Chaoui A, Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. Journal of Plant Nutrition 24, 1085–1097.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boisleve F, Kerdine-Römera S, Pallardya M (2005) Implication of the MAPK pathways in the maturation of human dendritic cells induced by nickel and TNF-α. Toxicology 206, 233–244.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. The New Phytologist 156, 205–215.
Crossref | GoogleScholarGoogle Scholar | open url image1

Camejo D, Jimenez A, Alarcon JJ, Torres W, Gomez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Functional Plant Biology 33, 177–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chatelier A, Renaudon B, Bescond J, Chemaly AE, Demion M, Bois P (2005) Calmodulin antagonist W7 directly inhibits f-type current in rabbit sino-atrial cells. European Journal of Pharmacology 521, 29–33.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Elstner EF (1991) Oxygen radicals-biochemical basis for their efficacy. Klinische Wochenschrift 69, 949–956.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. The Plant Cell 16, 2176–2191.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gajewska E, Słaba M, Andrzejewska R, Skłodowska M (2006) Nickel-induced inhibition of wheat root growth is related to H2O2 production, but not to lipid peroxidation. Plant Growth Regulation 49, 95–103. open url image1

Gardiner J, Collings DA, Harper JDI, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant & Cell Physiology 44, 687–696.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gomes-Junior RA, Moldes CA, Delite FS, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006) Nickel elicits a fast antioxidant response in Coffea arabica cells. Plant Physiology and Biochemistry 44, 420–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology 32, 481–494.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harmon AC, Yoo BC, McCaffery C (1994) Pseudosubstrate inhibition of CDPK, a protein kinase with a calmodulin-like domain. Biochemistry 33, 7278–7287.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 180–198. open url image1

Henmi K, Tsuboi S, Demura T, Fukuda H, Iwabuchi M, Ogawa KI (2001) A possible role of glutathione and glutathione disulfide in tracheary element differentiation in the cultured mesophyll cells of Zinnia elegans. Plant & Cell Physiology 42, 673–676.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Herskowitz I (1995) MAP kinase pathways in yeast: for mating and more. Cell 80, 187–197.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hideg E, Rosenqvist E, Varadi G, Bornman J, Vincze E (2006) A comparison of UV-B induced stress responses in three barley cultivars. Functional Plant Biology 33, 77–90.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiology 136, 3276–3283.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ichimura K, Tena G, Henry Y, Zhang Z, Hirt H, Wilson C, Morris P, Mundy J, Innes R, Ecker J (2002) Mitogen-activated protein kinase cascade in plants: a new nomenclature. Trends in Plant Science 7, 301–308.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ingram JL, Rice AB, Santos J, Van-Houten B, Bonner JC (2003) Vanadium-induced HB-EGF expression in human lung fibroblass is oxidant dependent and requires MAP kinases. American Journal of Physiology. Lung Cellular and Molecular Physiology 284, L774–L782.
PubMed |
open url image1

Jasper I, Samet JM, Erzurum S, Redd W (2000) Vanadium-induced kappaB-dependent transcription depends upon peroxide-induced activation of the p38 mitogen-activated protein kinase. American Journal of Respiratory Cell and Molecular Biology 23, 95–102.
PubMed |
open url image1

Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDδ, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. The Plant Journal 26, 595–605.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kukkola E, Rautio P, Huttunen S (2000) Stress indications in copper- and nickel-exposed Scots pine seedlings. Environmental and Experimental Botany 43, 197–210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee S, Suh S, Kim S, Crain RC, Kwak JM, Nam HG, Lee Y (1997) Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. The Plant Journal 12, 547–556.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lin CW, Chang HB, Huang HJ (2005) Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots. Plant Physiology and Biochemistry 43, 963–968.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paruch S, El-Benna J, Djerdjouri B, Marullo S, Perianin A (2006) A role of p44/42 mitogen-activated protein kinases in formyl-peptide receptor-mediated phospholipase D activity and oxidant production. The FASEB Journal 20, 142–144.
PubMed |
open url image1

Poulik Z (1997) The danger of accumulation of nickel in cereals on contaminated soil. Agriculture Ecosystems & Environment 63, 25–29.
Crossref | GoogleScholarGoogle Scholar | open url image1

Samet JM, Graves LM, Quay J, Dailey LA, Devlin RB, Ghio AJ, Wu W, Bromberg PA, Reed W (1998) Activation of MAPKs in human bronchial epithelial cells exposed to metals. American Journal of Physiology. Lung Cellular and Molecular Physiology 275, L551–L558. open url image1

Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant Journal 31, 629–638.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schickler H, Caspi H (1999) Response of antioxidant enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiologia Plantarum 105, 39–44.
Crossref | GoogleScholarGoogle Scholar | open url image1

Seo SR, Chong SA, Lee SI, Sung JY, Ahn YS, Chung KC, Seo JT (2001) Zn2+-induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. Journal of Neurochemistry 78, 600–610.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 53, 285–308. open url image1

Tsai TM, Huang HJ (2006) Effects of iron excess on cell viability and mitogen-activated protein kinase activation in rice roots. Physiologia Plantarum 127, 583–592.
Crossref | GoogleScholarGoogle Scholar | open url image1

Watanabe H, Yokozeki T, Yamazaki M, Miyazaki H, Sasaki T, Maehama T, Itoh K, Frohman MA, Kanaho Y (2004) Essential role for phospholipase D2 activation downstream of ERK MAP kinase in nerve growth factor-stimulated neurite outgrowth from PC12 Cells. Journal of Biological Chemistry 279, 37870–37877.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yamaguchi T, Tanabe S, Minami E, Shibuya N (2004) Activation of phospholipase D induced by hydrogen peroxide in suspension-cultured rice cells. Plant & Cell Physiology 45, 1261–1270.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yeh CM, Chien PS, Huang HJ (2007) Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. Journal of Experimental Botany 58, 659–671.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yeh CM, Hsiao LJ, Huang HJ (2004) Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant & Cell Physiology 45, 1306–1312.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yeh CM, Hung WC, Huang HJ (2003) Copper treatment activates mitogen-activated protein kinase signalling in rice. Physiologia Plantarum 119, 392–399.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yoshida S (1979) Freezing injury and phospholipid degradation in vivo in woody plant cells. III. Effect of freezing on activity of membrane-bound phospholipase D in microsome-enriched membrane. Plant Physiology 64, 252–256.
PubMed |
open url image1

Yuasa T, Ichimura K, Mizoguchi T, Shinozaki K (2001) Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant & Cell Physiology 42, 1012–1016.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang S, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9, 809–824.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1