Photosynthetica 2007, 45(2):272 | DOI: 10.1007/s11099-007-0044-y

Influence of irradiation on cyanide-resistant respiration and AOX1 multi-gene family expression during greening of etiolated rice seedlings

H. Q. Feng1, H. Y. Li1,*, G. M. Zhou2, H. G. Liang1, J. G. Duan1, D. J. Zhi1, X. Li1, J. Ma1
1 Department of Biochemistry and Molecular Biology, School of Life Science, Lanzhou University, Lanzhou, Peoples Republic of China
2 Biology Department, Brookhaven National Laboratory, Upton, USA

We investigated the differential expression of AOX1 multi-gene family and the regulation of alternative respiratory pathway during initial greening development in leaves of rice (Oryza sativa L.) seedlings. After exposing the dark-grown rice seedlings to continuous irradiation, total respiration (Vt), capacity of alternative pathway (Valt), and their ratio (Valt/Vt) increased with the greening of leaves. In this process, AOX1c transcript increased under constant irradiation, while AOX1a and AOX1b transcripts were hardly detected. Thus AOX1c in rice presents a similar expression pattern as AOX2 does in many dicotyledonous species during greening development. Compared with the rapid increase of cyanideresistant respiration in the presence of photon energy, CO2 fixation was not observed until 8 h after the onset of irradiation. The AOX inhibitor salicylhydroxamic acid (SHAM; 1 mM) inhibited 67.3 % of cyanide-insensitive oxygen uptake in dark-grown leaves and 69.4 % of it in leaves grown under irradiation. Dark-grown plants pre-treated with SHAM were then irradiated for 12 h. SHAM did not obviously modify photosynthetic CO2 fixation rate on a chlorophyll (Chl) content basis in both leaves and simultaneously isolated chloroplasts. Hence during initial greening steps of the plants, the induction of alternative pathway and AOX1 expression by irradiation is not directly linked with carbon assimilation of photosynthesis. The application of SHAM partially limited Chl production in rapidly greening leaves, indicating that Chl synthesis in the process of greening might be medicated to some extent by alternative respiratory pathway.

Additional key words: chlorophyll; chloroplast; CO2 fixation; inhibitors; Oryza; oxygen uptake; salicylhydroxamic acid

Received: May 12, 2006; Accepted: August 31, 2006; Published: June 1, 2007  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Feng, H.Q., Li, H.Y., Zhou, G.M., Liang, H.G., Duan, J.G., Zhi, D.J., Li, X., & Ma, J. (2007). Influence of irradiation on cyanide-resistant respiration and AOX1 multi-gene family expression during greening of etiolated rice seedlings. Photosynthetica, 45(2), 272. doi: 10.1007/s11099-007-0044-y
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Akerlund, P., Larsson, C., Widell, S., Møller, I.M.: NAD(P)H oxidase and peroxidase activities in purified plasma membranes from cauliflower inflorescences.-Physiol. Plant. 71: 9-19, 1987. Go to original source...
    2. Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.-Plant Physiol. 24: 1-15, 1949. Go to original source...
    3. Azcón-Bieto, J., Lambers, H., Day, D.A.: Effect of photosynthesis and carbohydrate status on respiratory rates and the involvement of the alternative oxidase pathway in leaf respiration.-Plant Physiol. 72: 598-603, 1983. Go to original source...
    4. Baker, N.R.: Development of chloroplast photochemical functions.-In: Baker, N.R., Barber, J. (ed.): Chloroplast Biogenesis. Pp. 207-251. Elsevier, Amsterdam 1984.
    5. Bartoli, C.G., Gomez, F., Gergoff, G., Guiamét, J.J., Puntarulo, S.: Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions.-J. exp. Bot. 56: 1269-1276, 2005. Go to original source...
    6. Bingham, I.J., Farrar, J.F.: Activity and capacity of respiration pathways in barley roots deprived of inorganic nutrients.-Plant Physiol. Biochem. 27: 847-854, 1989.
    7. Bingham, I.J., Stevenson, E.A.: Causes and location of non-specific effects of SHAM on O2 uptake by wheat roots.-Physiol. Plant. 93: 427-434, 1995. Go to original source...
    8. Bradbeer, J.W.: Development of photosynthetic function during chloroplast biogenesis.-In: Hatch, M.D., Boardman, N.K. (ed.): The Biochemistry of Plants. Vol. 8. Pp. 423-472. Academic Press, New York-London-Toronto-Sydney-San Francisco 1981. Go to original source...
    9. Bruick, R.K., Mayfield, S.P.: Light-activated translation of chloroplast mRNAs.-Trends Plant Sci. 4: 190-195, 1999. Go to original source...
    10. Chivasa, S., Carr, J.P.: Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase.-Plant Cell 10: 1489-1498, 1998. Go to original source...
    11. Chivasa, S., Murphy, A.M., Naylor, M., Carr, J.P.: Salicylic acid interferes with tobacco mosaic virus replication via a novel salicylhydroxamic acid-sensitive mechanism.-Plant Cell 9: 547-557, 1997. Go to original source...
    12. Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A., Whelan, J.: Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana.-Plant mol. Biol. 58: 193-212, 2005. Go to original source...
    13. Considine, M.J., Holtzapffel, R.C., Day, D.A., Whelan, J., Millar, A.H.: Molecular distinction between alternative oxidase from monocots and dicots.-Plant Physiol. 129: 949-953, 2002. Go to original source...
    14. Day, D.A., Wiskich, J.T.: Regulation of alternative oxidase activity in higher plants.-J. Bioenerg. Biomembr. 27: 379-385, 1995. Go to original source...
    15. Diethelm, R., Miller, M.G., Shibles, R., Stewart, C.R.: Effect of salicylhydroxamic acid on respiration, photosynthesis, and peroxidase activity in various plant tissues.-Plant Cell Physiol. 31: 179-185, 1990.
    16. Escobar, M.A., Franklin, K.A., Svensson, A.S., Salter, M.G., Whitelam, G.C., Rasmusson, A.G.: Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type IINAD(P)H dehydrogenase genes.-Plant Physiol. 136: 2710-2721, 2004. Go to original source...
    17. Finnegan, P.M., Whelan, J., Millar, A.H., Zhang, Q., Smith, M.K., Wiskich, J.T., Day, D.A.: Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase.-Plant Physiol. 114: 455-466, 1997. Go to original source...
    18. Gregory P., Bradbeer, J.W.: Plastid development in primary leaves of Phaseolus vulgaris.-Biochem. J. 148: 433-438, 1975. Go to original source...
    19. Gyldenholm, A.O., Whatley, F.: The onset of photophosphorylation in chloroplasts isolated from developing bean leaves.-New Phytol. 67: 461-468, 1986. Go to original source...
    20. Harris, M., Mackender, R.O., Smith, D.L.: Photosynthesis of cotyledons of soybean seedlings.-New Phytol. 104: 319-329, 1986. Go to original source...
    21. Hoefnagel, M.H.N., Atkin, O.K., Wiskich, J.T.: Interdependence between chloroplasts and mitochondria in the light and the dark.-Biochim. biophys. Acta 1366: 235-255, 1998. Go to original source...
    22. Lennon, A.M., Pratt, J., Leach, G., Moore, A.L.: Developmental regulation of respiratory activity in pea leaves.-Plant Physiol. 107: 925-932, 1995. Go to original source...
    23. Lurie, S.: Stomatal opening and photosynthesis in greening leaves of Vicia faba L.-Aust. J. Plant Physiol. 4: 69-74, 1977. Go to original source...
    24. Mackenzie, S., McIntosh, L.: Higher plant mitochondria.-Plant Cell 11: 571-586, 1999. Go to original source...
    25. Mahmudov, Z.M., Abdullayev, K.D.: Photoinhibition of photosystem II in vivo during greening of the wheat seedlings.-Turk. J. Bot. 29: 77-82, 2005.
    26. McCade, T.C., Finnegan, P.M., Millar, A.H., Day, D.A., Whelan, J.: Different expression of alternative oxidase genes in soybean cotyledons during postgerminative development.-Plant Physiol. 118: 675-682, 1998. Go to original source...
    27. Millenaar, F.F., Lambers, H.: The alternative oxidase: in vivo regulation and function.-Plant Biol. 5: 2-15, 2003. Go to original source...
    28. Møller, I.A., Bérczi, A., van der Plas, L.H.W., Lambers, H.: Measurement of the activity and capacity of the alternative pathway in intact plant tissues: identification of problems and possible solutions.-Physiol. Plant. 72: 642-649, 1988. Go to original source...
    29. Naylor, M., Murphy, A.M., Berry, J.O., Carr, J.P.: Salicylic acid can induce resistance to plant virus movement.-Mol. Plant-Microbe Interact. 11: 860-868, 1998. Go to original source...
    30. Obenland, D., Diethelm, R., Shibles, R., Stewart, C.: Relationship of alternative respiratory capacity and alternative oxidase amount during soybean seedling growth.-Plant Cell Physiol. 31: 897-901, 1990.
    31. Padmasree, K., Padmavathi, L., Raghavendra, A.S.: Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition.-Crit. Rev. Biochem. mol. Biol. 37: 71-119, 2002. Go to original source...
    32. Padmasree, K., Raghavendra, A.S.: Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: Metabolites related to the redox status and sucrose biosynthesis.-Photosynth. Res. 62: 231-239, 1999. Go to original source...
    33. Phung Nhu Hung, S., Hoarau, A., Moyse, A.: Étude de l'évolution en chloroplasts des plastes etioles d'orge. II. Photophosphorylation et photoréduction du NADP, formation de ferrédoxine, en éclairement continue et par l'action d'éclairs.-Z. Pflanzenphysiol. 62: 245-250, 1970.
    34. Raghavendra, A.S., Padmasree, K.: Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation.-Trends Plant Sci. 8: 546-553, 2003. Go to original source...
    35. Ribas-Carbo, M., Robinson, S.A., Gonzalez-Meler, M.A., Lennon, A.M., Giles, L., Siedow, J.N., Berry, J.A.: Effects of light on respiration and oxygen isotope fractionation in soybean cotyledons.-Plant Cell Environ. 23: 983-989, 2000. Go to original source...
    36. Saika, H., Ohtsu, K., Hamanaka, S., Nakazono, M.: AOX1c, a novel rice gene for alternative oxidase, comparison with rice AOX1a and AOX1b.-Genes genet. Syst. 77: 31-38, 2002. Go to original source...
    37. Saisho, D., Nakazono, M., Lee, K.H., Tsutsumi, N., Akita, S., Hirai, A.: The gene for alternative oxidase-2 (AOX-2) from Arabidopsis thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination.-Genes genet. Syst. 76: 89-97, 2001. Go to original source...
    38. Svensson, Å.S., Rasmusson, A.G.: Light-dependent gene expression for proteins in the respiratory chain of potato leaves.-Plant J. 28: 1-73, 2001. Go to original source...
    39. Takumi, S., Tomioka, M., Eto, K., Naydenow, N., Nakamura, C.: Characterization of two non-homoeologous nuclear genes encoding mitochondrial alternative oxidase in common wheat.-Genes genet. Syst. 71: 77-88, 2002. Go to original source...
    40. Vanlerberghe, G.C., Alison, E., McIntosh, L.: Molecular genetic evidence of the ability of alternative oxidase to support respiratory carbon metabolism.-Plant Physiol. 113: 657-661, 1997. Go to original source...
    41. Vanlerberghe, G.C., McIntosh, L.: Mitochondrial electron transport regulation of nuclear gene expression: studies with the alternative oxidase gene of tobacco.-Plant Physiol. 105: 867-874, 1994. Go to original source...
    42. Vanlerberghe, G.C., McIntosh, L.: Alternative oxidase: from gene to function.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 703-734, 1997. Go to original source...
    43. Van Lis, R., Atteia, A.: Control of mitochondrial function via photosynthetic redox signals.-Photosynth. Res. 79: 133-148, 2004. Go to original source...
    44. Whelan, J., Smith, M.K., Meijer, M., Yu, J.W., Badger, M.R., Price, G.D., Day, D.A.: Cloning of an additional cDNA for alternative oxidase in tobacco.-Plant Physiol. 107: 1469-1470, 1995. Go to original source...

    Return to the content