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Inhibition of ribonuclease and protease activities in germinating rice seeds exposed to nickel

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Abstract

When the seeds of two rice cvs. Malviya-36 and Pant-12 were germinated up to 120 h in the presence of 200 and 400 μM NiSO4, a significant reduction in the germination of seeds occurred. Seeds germinating in the presence of 400 μM NiSO4 showed about 12–20% decline in germination percent, about 20–53% decline in lengths and about 8–34% decline in fresh weights of roots and shoots at 120 h of germination. Ni2+ exposure of germinating seeds resulted in apparent increased levels of RNA, soluble proteins, and free amino acids in endosperms as well as embryo axes. A 400 μM Ni2+ treatment led to about 58–101% increase in the level of soluble proteins and about 39–107% increase in the level of free amino acids in embryo axes at 96 h of germination. Activities of ribonuclease and protease declined significantly with increasing levels of Ni2+ treatment. Isoenzyme profile of RNase as revealed by activity staining indicated decline in the intensities of 3–4 preexisting enzyme isoforms in embryo axes of both the rice cultivars and disappearance of one of the two isoforms in endosperms of cv. Pant-12 due to 400 μM Ni2+ treatment. Results suggest that the presence of high level of Ni2+ in the medium of germinating rice seeds serves as a stress factor resulting in decreased hydrolysis as well as delayed mobilization of endospermic RNA and protein reserves and causing imbalance in the level of biomolecules like RNA, proteins, and amino acids in growing embryo axes. These events would ultimately contribute to decreased germination of rice seeds in high Ni2+ containing environment.

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References

  • Ahsan N, Lee DG, Lee SH, Kang KY, Lee JJ, Kim PJ et al (2007) Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67:1182–1193. doi:10.1016/j.chemosphere.2006.10.075

    Article  PubMed  CAS  Google Scholar 

  • Alia, Saradhi PP (1991) Proline accumulation under heavy metal stress. J Plant Physiol 138:554–558

  • Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64. doi:10.1071/FP02074

    Article  CAS  Google Scholar 

  • Bewley JD, Black M (1994) Seeds: physiology of development and germination, 2nd edn. Plenum Press, New York, pp 293–310

    Google Scholar 

  • Booker FL (2004) Influence of ozone on ribonuclease activity in wheat (Triticum aestivum) leaves. Physiol Plant 120:249–255. doi:10.1111/j.0031-9317.2004.0238.x

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Chang S-C, Gallie DR (1997) RNase activity decreases following a heat shock in wheat leaves and correlates with its posttranslational modification. Plant Physiol 113:1253–1263

    PubMed  CAS  Google Scholar 

  • Chen CT, Chen LM, Lin CC, Kao CH (2001) Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Sci 160:283–290. doi:10.1016/S0168-9452(00)00393-9

    Article  PubMed  CAS  Google Scholar 

  • Choi SB, Wang C, Muench DG, Ozawa K, Franceschi VR, Wu Y et al (2000) Messenger RNA targeting of rice seed storage proteins to specific ER subdomains. Nature 407(6805):765–767. doi:10.1038/35037633

    Article  PubMed  CAS  Google Scholar 

  • Davis BJ (1964) Disc electrophoresis II. Method and application to human serum protein. Ann N Y Acad Sci 121:404–427. doi:10.1111/j.1749-6632.1964.tb14213.x

    Article  PubMed  CAS  Google Scholar 

  • Dubey RS (1982) Biochemical changes in germinating rice seeds under saline stress. Biochem Physiol Pflanz 177:523–535

    CAS  Google Scholar 

  • Dubey RS, Rani M (1989) Salinity induced accumulation of free amino acids in germinating rice seeds differing in salt tolerance. J Agron Crop Sci 163:236–247. doi:10.1111/j.1439-037X.1989.tb00763.x

    Article  CAS  Google Scholar 

  • Espen L, Pirovano L, Cocucci SM (1997) Effect of Ni2+ during the early phases of radish (Raphnus sativus) seed germination. Environ Exp Bot 38:187–197. doi:10.1016/S0098-8472(97)00011-7

    Article  CAS  Google Scholar 

  • Fincher GB (1989) Molecular and cellular biology association with endosperm mobilization in germination cereal grains. Annu Rev Plant Physiol Plant Mol Biol 40:305–346. doi:10.1146/annurev.pp. 40.060189.001513

    Article  CAS  Google Scholar 

  • Gabbrielli R, Pandolfini T, Espen L, Palandri MR (1999) Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J Plant Physiol 155:639–645

    CAS  Google Scholar 

  • Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848

    Article  PubMed  CAS  Google Scholar 

  • Gianazza E, Wait R, Sozzi A, Regondi S, Saco D, Labra M et al (2007) Growth and protein profile changes in Lepidium sativum L. plantlets exposed to cadmium. Environ Exp Bot 59:179–187. doi:10.1016/j.envexpbot.2005.12.005

    Article  CAS  Google Scholar 

  • Gomes-Filho E, Lima CRFM, Enéas-Filho J, Gondim LA, Prisco JT (1999) Purification and properties of a ribonuclease from cowpea cotyledons. Biol Plant 42:525–532. doi:10.1023/A:1002602712392

    Article  CAS  Google Scholar 

  • Grilli I, Meletti P, Spanò C (2002) Ribonucleases during ripining and after-ripening in Triticum durum embryos. J Plant Physiol 159:935–937. doi:10.1078/0176-1617-00568

    Article  CAS  Google Scholar 

  • Gupta R, Shetrapal KS, Jain U, Soni D (2001) Effect of copper and nickel on seed germination and seedling growth of Raphanus sativus Var. Pusa Chetki. Indian J Environ Sci 5(1):93–96

    Google Scholar 

  • Herman EM, Larkins BA (1999) Protein storage bodies and vacuoles. Plant Cell 11:601–613

    Article  PubMed  CAS  Google Scholar 

  • Jha AB, Dubey RS (2005) Effect of arsenic on behaviour of enzymes of sugar metabolism in germinating rice seeds. Acta Physiol Plant 27(3B):341–348. doi:10.1007/s11738-005-0010-x

    Article  CAS  Google Scholar 

  • Krupa Z, Siedlecka A, Maksymiec W, Baszyñski T (1993) In vivo response of photosynthetic apparatus of Phaseolus vulgaris L. to nickel toxicity. J Plant Physiol 142:664–668

    CAS  Google Scholar 

  • Kuriakose SV, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156. doi:10.1007/s10725-007-9237-4

    Article  CAS  Google Scholar 

  • Larcher W (1995) The utilization of mineral elements. In: Larcher W (ed) Physiological plant ecology, 3rd edn. Springer, Berlin, pp 167–213

    Google Scholar 

  • Leon V, Rabier J, Notonier R, Barthelémy R, Moreau X, Bouraïma-Madjèbi S et al (2005) Effects of three nickel salts on germinating seeds of Grevillea exul var. rubiginosa, an endemic serpentine proteaceae. Ann Bot (Lond) 95:609–618. doi:10.1093/aob/mci066

    Article  CAS  Google Scholar 

  • Li W, Khan MA, Yamaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul 46:45–50. doi:10.1007/s10725-005-6324-2

    Article  CAS  Google Scholar 

  • Lin Y, Kao C (2006) Effects of excess nickel on starch mobilization in germinating rice grains. J Plant Nutr 29:1405–1412. doi:10.1080/01904160600830225

    Article  CAS  Google Scholar 

  • Lowry OH, Rosenbrough JJ, Farr AL, Randall RJ (1951) Estimation of protein with the folin phenol reagent. J Biol Chem 193:265

    PubMed  CAS  Google Scholar 

  • Maheshwari R, Dubey RS (2007) Nickel toxicity inhibits ribonuclease and protease activities in rice seedlings: protective effects of proline. Plant Growth Regul 51:231–243. doi:10.1007/s10725-006-9163-x

    Article  CAS  Google Scholar 

  • Mihoub A, Chaoui A, Ferjani EE (2005) Biochemical change associated with cadmium and copper stress in germinating pea seeds (Pisum sativum L.). C R Biol 328:33–41

    Article  PubMed  CAS  Google Scholar 

  • Mishra S, Dubey RS (2006) Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: Role of proline as enzyme protectant. J Plant Physiol 163:927–936. doi:10.1016/j.jplph.2005.08.003

    Article  PubMed  CAS  Google Scholar 

  • Mittal R, Dubey RS (1991) Influence of salinity on ribonuclease activity and status of nucleic acids in rice seedlings differing in salt tolerance. Plant Physiol Biochem 18:57–64

    Google Scholar 

  • Nagoor S, Vyas AV (1999) Physiological and bio-chemical responses of cereal seedlings to graded levels of heavy metals. III. Effects of copper on protein metabolism in wheat seedlings. J Environ Biol 20:125–129

    CAS  Google Scholar 

  • Osborne DJ (1993) Function of DNA synthesis and DNA repair in the survival of embryos during early germination and in dormancy. Seed Sci Res 3:43–53

    Google Scholar 

  • Palma JM, Sandalio LM, Corpas FJ, Romero-Puertas MC, McCarthy I, del Río LA (2002) Plant protease, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40:521–530. doi:10.1016/S0981-9428(02)01404-3

    Article  CAS  Google Scholar 

  • Parida BK, Chhibba IM, Nayyer VK (2003) Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci Hortic (Amsterdam) 98:113–119. doi:10.1016/S0304-4238(02)00208-X

    Article  CAS  Google Scholar 

  • Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea [Cajanus cajan (L.) Millspaugh] in response to Zn and Ni stresses. Plant Sci 157:113–128. doi:10.1016/S0168-9452(00)00273-9

    Article  Google Scholar 

  • Rosen H (1959) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67:10–15. doi:10.1016/0003-9861(57)90241-2

    Article  Google Scholar 

  • Rout GR, Samantaray S, Das P (2000) Effects of chromium and nickel on germination and growth in tolerant and non-tolerant populations of Echinochloa colona (L.) link. Chemosphere 40:855–859. doi:10.1016/S0045-6535(99)00303-3

    Article  PubMed  CAS  Google Scholar 

  • Schneider WC (1957) Determination of nucleic acids by pentose analysis. Methods Enzymol 3:680–684. doi:10.1016/S0076-6879(57)03442-4

    Article  Google Scholar 

  • Shah K, Dubey RS (1995) Cadmium induced changes on germination, RNA level and ribonuclease activity in rice seeds. Plant Physiol Biochem N Delhi 22:101–107

    Google Scholar 

  • Shah K, Dubey RS (1998) Cadmium elevates level of protein, amino acids and alters the activity of proteolytic enzymes in germinating rice seeds. Acta Physiol Plant 20:189–196. doi:10.1007/s11738-998-0013-5

    Article  CAS  Google Scholar 

  • Spanò C, Crosatti C, Pacchini R, Meletti P, Grilli I (2002) Ribonucleases during cold acclimation in winter and spring wheats. Plant Sci 162:809–815. doi:10.1016/S0168-9452(02)00026-2

    Article  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206. doi:10.1111/j.1365-3040.1990.tb01304.x

    Article  Google Scholar 

  • Volkin E, Cohn WE (1954) Estimation of nucleic acid. In: Click G (ed) Methods of biochemical analysis. Interscience, New York, pp 287–306

    Chapter  Google Scholar 

  • Yamauchi D (2003) Regulation of gene expression of a cysteine proteinase, EP-C1, by a VIVIPAROUS1-like factor from common bean. Plant Cell Physiol 44:649–652. doi:10.1093/pcp/pcg076

    Article  PubMed  CAS  Google Scholar 

  • Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82. doi:10.1080/713608066

    Article  CAS  Google Scholar 

  • Wilson CM (1967) Purification of a corn ribonuclease. J Biol Chem 242:2260–2263

    PubMed  CAS  Google Scholar 

  • Zhang N, Jones B (1999) Polymorphism of aspartic proteinases in resting and germinating barley seeds. Cereal Chem 76:134–138. doi:10.1094/CCHEM.1999.76.1.134

    Article  CAS  Google Scholar 

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Correspondence to Rama S. Dubey.

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Communicated by S. Weidner.

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Maheshwari, R., Dubey, R.S. Inhibition of ribonuclease and protease activities in germinating rice seeds exposed to nickel. Acta Physiol Plant 30, 863–872 (2008). https://doi.org/10.1007/s11738-008-0192-0

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  • DOI: https://doi.org/10.1007/s11738-008-0192-0

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