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. 2008 Sep 27;14(3):235–251. doi: 10.1007/s12298-008-0023-1

The alternative oxidase mediated respiration contributes to growth, resistance to hyperosmotic media and accumulation of secondary metabolites in three species

V Sitaramam 1,✉, Shilpa Pachapurkar 1, Trupti Gokhale 1
PMCID: PMC3550620  PMID: 23572891

Abstract

Plant respiration, similar to respiration in animal mitochondria, exhibits both osmosensitive and insensitive components with the clear distinction that the insensitive respiration in plants is quantitatively better described as ‘less’ sensitive rather than ‘insensitive’. Salicylic hydroxamic acid (SHAM)-sensitive respiration was compared with the respiration sensitive to other inhibitors in rice, yeast and Dunaliella salina. The influence of SHAM was largely in the osmotically less sensitive component and enhanced with external osmotic pressure unlike other inhibitors that inhibited the osmotically sensitive component. SHAM inhibited germination and root growth but not shoot growth. Osmotic remediation of respiration that developed in due course of time with rice seedlings was abolished by SHAM and was not due to water and ionic uptake mechanisms. Yeast and Dunaliella also showed susceptibility of growth and respiration to SHAM. Glycerol retention was influenced by all inhibitors, while growth was inhibited demonstrably by SHAM in Dunaliella. Respiration in plants needs to be seen as a positive contribution to overall growth and not merely for burning away of the biomass.

Key words: SHAM, inhibitors of respiration, yeast, rice, Dunaliella, osmotic sensitivity, voids

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Abbreviations

SHAM

salicylhydroxamic acid

References

  1. Ben-Amotz A., Sussman I., Avron M. Glycerol production by Dunaliella Experientia. 1982;38:49–52. [Google Scholar]
  2. Brown A.D., Lilley R.Mc.C., Marengo T. Osmorregulation in Dunaliella. Intracellular distribution of enzymes of glycerol metabolism. Plant Physiol. 1982;53:628–631. [Google Scholar]
  3. Chong P.L.G., Fortes P.A.G., Jameson D.M. Mechanism of inhibition of (Na, K)-ATPase by hydrostatic pressure studied with fluorescence probes. J. Biol. Chem. 1985;260:14484–14490. [PubMed] [Google Scholar]
  4. Cournac L., Latouche G., Cerovic Z., Redding K., Ravenel J., Peltier G. In vivo interactions between photosynthesis, mitorespiration and chlororespiration in Chlamydomonas reinhardtii. 2002;129:1921–1928. doi: 10.1104/pp.001636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Falck E., Patra M., Karttunen M., Hyvänen M.T., Vattulainen I. Response to Comment by Almeida et al.: Free Area Theories for Lipid Bilayers—Predictive or Not? Biophys. J. 2005;89:745–752. doi: 10.1529/biophysj.105.065714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hoagland, D. and Arnon, D. (1950). The water-culture method for growing plants without soil. Calif. Agric. Expt. Sta. Cir. 347.
  7. Izawa S. Methods Enzymol. N.Y.: Acedemic press; 1980. Acceptors and donors for chloroplast electron transport; pp. 413–434. [Google Scholar]
  8. Joet T., Cournac L., Horvath E., Medgyesy P., Peltier G. Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around Photosystem I. Plant Physiol. 2001;125:1919–1929. doi: 10.1104/pp.125.4.1919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. McDonald A.E., Sieger S.M., Vanlerberghe G.C. Methods and approaches to study plant mitochondrial alternative oxidase. Physiologia Plantarum. 2002;116:135–143. doi: 10.1034/j.1399-3054.2002.1160201.x. [DOI] [PubMed] [Google Scholar]
  10. Madhavarao C.N., Sauna Z.E., Sitaramam V. Solvent interconnectedness permits measurement of proximal as well as distant phase transitions in polymer mixtures by fluorescence. Biophysical Chemistry. 2000;90:147–156. doi: 10.1016/S0301-4622(01)00136-3. [DOI] [PubMed] [Google Scholar]
  11. Madhavarao C.N., Sauna Z.E., Srivatsava A., Sitaramam V. Osmotic perturbations induce differential movements in the core and periphery of proteins, membranes and micelles. Biophysical Chemistry. 2001;90:231–246. doi: 10.1016/s0301-4622(01)00144-2. [DOI] [PubMed] [Google Scholar]
  12. Mathai J.C., Sitaramam V. Variable porosity of the mitochondrial inner membrane induced by energization. Biochim. Biophys. Acta. 1989;976:214–221. doi: 10.1016/S0005-2728(89)80233-6. [DOI] [PubMed] [Google Scholar]
  13. Mathai J.C., Sauna Z.E., John O., Sitaramam V. Rate limiting step in electron transport: osmotically sensitive diffusion of quinones through voids in the bilayer. J. Biol. Chem. 1993;268:15442–15454. [PubMed] [Google Scholar]
  14. Mathai J.C., Sitaramam V. Stretch sensitivity of transmembrane mobility of hydrogen peroxide through voids in the bilayer: role of cardiolipin. J. Biol. Chem. 1994;269:17784–17793. [PubMed] [Google Scholar]
  15. Meeuse B.J.D. Thermogenic respiration in Aroids. Annual Rev. Plant Physiol. 1975;26:117–126. doi: 10.1146/annurev.pp.26.060175.001001. [DOI] [Google Scholar]
  16. Millar A.H., Atkins O.K., Menz I., Henry B., Fraquhar G., Day D.A. Analysis of respiratory chain regulation in roots of Soybean seedlings. Plant Physiol. 1998;117:1083–1093. doi: 10.1104/pp.117.3.1083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Munn R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25:239–250. doi: 10.1046/j.0016-8025.2001.00808.x. [DOI] [PubMed] [Google Scholar]
  18. Natesan S., Madhavarao C.N., Sitaramam V. The positive role of voids in the plasma membrane in growth and energetics of Escherischia coli. Biophysical Chemistry. 2000;85:59–78. doi: 10.1016/S0301-4622(00)00145-9. [DOI] [PubMed] [Google Scholar]
  19. Pan R.S., Sauna Z., Dilley R.A., Sitaramam V. Influence of osmolality of the medium on photosynthetic electron transport. Proton fluxes and photophosphorylation in isolated thylakoids. Indian J. Biochem. and Biophys. 1995;32:1–10. [PubMed] [Google Scholar]
  20. Parsegian V.A., Rand R.P., Fuller N.L., Rau D.C. Osmotic stress for direct measurement of intermolecular forces. Methods in Enzymol. 1986;127:400–416. doi: 10.1016/0076-6879(86)27032-9. [DOI] [PubMed] [Google Scholar]
  21. Penning De Vries F.W.T. The cost of maintenance processes in plant cells. Ann. Bot. 1975;36:77–92. [Google Scholar]
  22. Pradhan G.R., Pandit S.A., Gangal A.D., Sitaramam V. Effect of shape anisotropy on transport in a two-dimensional computational model:numerical simulations showing experimental features observed in biomembranes. Physica A. 1999;270:288–294. doi: 10.1016/S0378-4371(99)00130-2. [DOI] [Google Scholar]
  23. Pradhan G.R., Pandit S.A., Gangal A.D., Sitaramam V. Shape anisotropy of lipid molecules and voids. J.Theoret. Biol. 2003;220:189–199. doi: 10.1006/jtbi.2003.3155. [DOI] [PubMed] [Google Scholar]
  24. Rajagopal K., Sitaramam V. Biology of the inner space: voids in biopolymers. J. Theor. Biol. 1998;195:245–271. doi: 10.1006/jtbi.1998.0786. [DOI] [PubMed] [Google Scholar]
  25. Rand R.P., Fuller N.L., Butko P., Francis G., Nicholls P. Measured change in protein solvation with substrate binding and turnover. Biochem. 1993;32:5925–5929. doi: 10.1021/bi00074a001. [DOI] [PubMed] [Google Scholar]
  26. Sambasivarao D., Kramer R., Rao N.M., Sitaramam V. ATP hydrolysis induces variable porosity to mannitol in the mitochondrial inner membrane. Biochim. Biophys. Acta. 1988;933:200–211. doi: 10.1016/0005-2728(88)90071-0. [DOI] [PubMed] [Google Scholar]
  27. Sauna Z.E., Madhavarao C.N., Sitaramam V. Large solutes induce structural perturbations in proteins and membranes. Int. J. Biol. Macromolecules. 2001;29:5–18. doi: 10.1016/S0141-8130(01)00147-7. [DOI] [PubMed] [Google Scholar]
  28. Shanubhogue A., Rajarshi M.B., Gore A.P., Sitaramam V. Statistical testing of equality of two breakpoints in experimental data. J. Biochem. Biophys. Methods. 1992;25:95–112. doi: 10.1016/0165-022X(92)90002-R. [DOI] [PubMed] [Google Scholar]
  29. Sitaramam V., Madhavarao C.N. The energetic basis of osmotolerance in plants: Physical Principles. J theoret Biol. 1997;189:333–352. doi: 10.1006/jtbi.1997.0522. [DOI] [PubMed] [Google Scholar]
  30. Sitaramam V., Sauna Z.E. What does a common channel for electrolytes and non-electrolytes in the sperm mean. J. Theoret. Biol. 2000;206:419–428. doi: 10.1006/jtbi.2000.2134. [DOI] [PubMed] [Google Scholar]
  31. Sitaramam V. Common fallacies in plant physiology in understanding osmotolerance: new methodology to define the phenotype. Physiol. Mol. Biol. Plants. 2006;12:107–123. [Google Scholar]
  32. Sitaramam V., Rao N.M., Bhate R. Osmotolerance in plants: phenotyping for osmotolerance in cultivars with differential requirement for water. Physiol. Mol. Biol. Plants. 2006;13:115–126. [Google Scholar]
  33. Sitaramam V., Atre V. Osmotolerance varies during life cycle of Arabidopsis. Physiol. Mol. Biol. Plants. 2007;13:127–136. [Google Scholar]
  34. Sitaramam V., Rao N.M. Osmotolerance in plants: respiration matches the ecological preference. Physiol. Mol. Biol. Plants. 2006;12:229–240. [Google Scholar]
  35. Slater M. Manometric methods and phosphate determination. Methods Enzymol. 1967;10:19–29. doi: 10.1016/0076-6879(67)10006-2. [DOI] [Google Scholar]
  36. Somogyi B., Welch G.R., Damjanovich S. The dynamic basis of energy transduction in enzymes. Biochim. Biophys. Acta. 1984;768:81–112. doi: 10.1016/0304-4173(84)90001-6. [DOI] [PubMed] [Google Scholar]
  37. Thornley J.H.M. Respiration, growth and maintenance in plants. Nature. 1970;227:304–305. doi: 10.1038/227304b0. [DOI] [PubMed] [Google Scholar]
  38. Thornley J.H.M. Energy respiration and growth in plants. Ann. Bot. 1971;35:721–728. [Google Scholar]
  39. Thornley J.H.M., Cannell M.G.R. Modelling the components of plant respiration and realism. Ann. Bot. 2000;85:55–67. doi: 10.1006/anbo.1999.0997. [DOI] [Google Scholar]
  40. Wagner A.M., Krab K. The alternative respiration pathways in plants: Role and regulation. Physiologia Plantarum. 1995;95:318–325. doi: 10.1111/j.1399-3054.1995.tb00844.x. [DOI] [Google Scholar]
  41. Yancy P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science. 1982;217:1214–1222. doi: 10.1126/science.7112124. [DOI] [PubMed] [Google Scholar]

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