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Mitochondrial activity in illuminated leaves of chlorophyll-deficient mutant rice (OsCHLH) seedlings

  • Goh, Chang-Hyo (Environmental Biotechnology National Core Research Center, Gyeongsang National University) ;
  • Satoh, Kouji (Department of Molecular Genetics, National Institute of Agrobiological Sciences) ;
  • Kikuchi, Shoshi (Department of Molecular Genetics, National Institute of Agrobiological Sciences) ;
  • Kim, Seong-Cheol (National Institute of Subtropical Agriculture, Rural Development Administration) ;
  • Ko, Suk-Min (Subtropical Horticulture Research Institute, Jeju National University) ;
  • Kang, Hong-Gyu (Subtropical Horticulture Research Institute, Jeju National University) ;
  • Jeon, Jong-Seong (Plant Metabolism Research Center and Graduate School of Biotechnology, Kyung Hee University) ;
  • Kim, Cheol-Soo (Department of Plant Biotechnology and Agricultural Plant Stress Research Center, Chonnam National University) ;
  • Park, Youn-Il (Department of Biology, Chungnam National University)
  • Received : 2010.07.18
  • Accepted : 2010.07.29
  • Published : 2010.12.30

Abstract

The rice CHLH gene encodes the $Mg^{2+}$-chelatase H subunit, which is involved in chlorophyll biosynthesis. Growth of the chlorophyll-deficient oschlh mutant is supported by mitochondrial activity. In this study, we investigated the activity of mitochondrial respiration in the illuminated leaves during oschlh seedling development. Growth of mutant plants was enhanced in the presence of 3% sucrose, which may be used by mitochondria to meet cellular energy requirements. ATP content in these mutants was, however, significantly lowered in light conditions. Low cytosolic levels of NADH in illuminated oschlh mutant leaves further indicated the inhibition of mitochondrial metabolism. This down-regulation was particularly evident for oxidative stressresponsive genes in the mutant under light conditions. Hydrogen peroxide levels were higher in oschlh mutant leaves than in wild-type leaves; this increase was largely caused by the impairment of the expression of the antioxidant genes, such as OsAPXl, OsRACl, and OsAOXc in knockout plants. Moreover, treatment of mesophyll protoplasts with ascorbic acid or catalase recovered ATP content in the mutants. Taken together, these results suggest that the light-mediated inhibition of mitochondrial activity leads to stunted growth of CHLH rice seedlings.

Keywords

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399 https://doi.org/10.1146/annurev.arplant.55.031903.141701
  2. Amirsadeghi S, McDonald AE, Vanlerberghe GC (2007) A glucocorticoid- inducible gene expression system can cause growth defects in tobacco. Planta 226:453-463 https://doi.org/10.1007/s00425-007-0495-1
  3. Atkin OK, Evans JR, Ball MC, Lambers H, Pons TL (2002) Leaf respiration of snow gum in the light and dark: interactions between temperature and irradiance. Plant Physiol 122:915-923
  4. Bartoli CG, Gomez F, Martinez DE, Guiamet J (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). J Exp Bot 55:1663-1669 https://doi.org/10.1093/jxb/erh199
  5. Bate GC, Siiltemeyer DF, Fock HP (1988) $^{16}O_{2}/^{18}O_{2}$ analysis of oxygen exchange in Dunaliella tertiolecta. Evidence for the inhibition of mitochondrial respiration in the light. Photosyn Res 16:219-231 https://doi.org/10.1007/BF00028841
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72:248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  7. Braidot E, Petrussa E, Vianello A, Macri F (1999) Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I or complex II substrates. FEBS Lett 451:347-350 https://doi.org/10.1016/S0014-5793(99)00616-X
  8. Brooks A, Farquhar GD (1985) Effect of temperature on the $CO_{2}-O_{2}$specificity of ribulose-1,5-biphosphate carboxylase/oxygenase and the rate of respiration in the light: estimates from gas exchange measurements on spinach. Planta 165:247-256
  9. Budde RJA, Randall DD (1990) Pea leaf mitochondrial PDH complex is inactivated in vivo in a light-dependent manner. Proc Natl Acad Sci USA 87:673-676 https://doi.org/10.1073/pnas.87.2.673
  10. Canvin DT, Berry JA, Badger MR, Fock H, Osmond CB (1980) $O_{2}$ exchange in leaves in the light. Plant Physiol 66:302-307 https://doi.org/10.1104/pp.66.2.302
  11. Chen M, Chory J, Fankhauser C (2004) Light signaling transduction in higher plants. Annu Rev Genet 38:87-117 https://doi.org/10.1146/annurev.genet.38.072902.092259
  12. Dat JF, Pellinen R, Van De Cotte B, Langebartels C, Kangasjarvi J, Inze D, Van breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621-632 https://doi.org/10.1046/j.1365-313X.2003.01655.x
  13. Day DA, Neuburger M, Douce R (1985) Interactions between glycine decarboxylase, the tricarboxylic acid cycle and the respiratory chain in pea leaf mitochondria. Aust J Plant Physiol 12:119-130 https://doi.org/10.1071/PP9850119
  14. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131:264-275 https://doi.org/10.1104/pp.011155
  15. Escobar MA, Franklin KA, Svensson AS, Salter MG, Whitelam GC, Rasmusson AG (2004) Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type II NAD(P)H dehydrogenase genes. Plant Physiol 136:2710-2721 https://doi.org/10.1104/pp.104.046698
  16. Feng W, Hongbin W, Bing L, Jinfa W (2006) Cloning and characterization of a novel splicing isoform of the iron-superoxide dismutanse gene in rice (Oryza sativa L.). Plant Cell Rep 24:734-742 https://doi.org/10.1007/s00299-005-0030-4
  17. Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254-261 https://doi.org/10.1016/j.pbi.2004.03.007
  18. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359-388 https://doi.org/10.1046/j.1469-8137.2000.00667.x
  19. Gao C, Xing D, Li L, Zhang L (2008) Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227:755-767 https://doi.org/10.1007/s00425-007-0654-4
  20. Gerbaud A, Andre M (1980) Effect of $CO_{2}$, $O_{2}$ and light on photosynthesis and photorespiration in wheat. Plant Physiol 66:1032-1036 https://doi.org/10.1104/pp.66.6.1032
  21. Goh CH, Jung KH, Roberts SK, McAinsh MR, Hetherington AM, Park Y, Suh K, An G, Nam HG (2004) Mitochondria provide the main source of cytosolic ATP for activation of outwardrectifying $K^{+}$ channels in mesophyll protoplast of chlorophylldeficient mutant rice seedlings. J Biol Chem 279:6874-6882
  22. Goh CH, Oh S, Moon YH, An G, Lee CH (2007) Activation of mitochondrial respiration in chlorophyll-deficient rice mutant seedlings. J Plant Biol 50:430-439 https://doi.org/10.1007/BF03030679
  23. Hill SA, Bryce JH (1992) Malate metabolism and light-enhanced dark respiration in barley mesophyll protoplasts. In: Lambers H, van der Plas LHW (eds) Molecular biochemical and physiological aspects of plant respiration. SPB Academy, The Hague, pp 221-230
  24. Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1366:235-255 https://doi.org/10.1016/S0005-2728(98)00126-1
  25. Igamberdiev AU, Gardestrom P (2003) Regulation of NAD and NADP dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim Biophys Acta 1606:117-125 https://doi.org/10.1016/S0005-2728(03)00106-3
  26. Islam MS, Niwa Y, Takagi S (2009) Light-dependent intracellular positioning of mitochondria in Arabidopsis thaliana mesophyll cells. Plant Cell Physiol 50:1032-1040 https://doi.org/10.1093/pcp/pcp054
  27. Journet EP, Bligny R, Douce R (1986) Biochemical changes during sucrose deprivation in higher plant cells. J Biol Chem 261:3193-3199
  28. Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An G (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 144:463-472
  29. Kari AS, McClintick A, Van Volkenburgh E (2003) A developmental gradient in the mechanism of $K^{+}$ uptake during light-stimulated leaf growth in Nicotiana tabacum L. Planta 217:587-596 https://doi.org/10.1007/s00425-003-1023-6
  30. Kleine T, Lockhart P, Batschauer A (2003) An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J 35:93-103 https://doi.org/10.1046/j.1365-313X.2003.01787.x
  31. Kromer S (1995) Respiration during photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 46:45-70 https://doi.org/10.1146/annurev.pp.46.060195.000401
  32. Lin M, Turpin DH, Plaxton WC (1989) Pyruvate kinase isozymes from the green alga Selenastrum minutum. Kinetic and regulatory properties. Arch Biochem Biophys 269:228-238 https://doi.org/10.1016/0003-9861(89)90104-5
  33. Loreto F, Velikova V, Di Marco G (2001) Respiration in the light measured by $^{12}CO_{2}$ emission in $^{13}CO_{2}$ atmosphere in maize leaves. Aust J Plant Physiol 28:1103-1108
  34. MacGregor DR, Deak KI, Ingram PA, Malamy JE (2008) Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues. Plant Cell 20:2643-2660 https://doi.org/10.1105/tpc.107.055475
  35. Minakuchi K, Yabushita T, Masumura T, Ichihara K, Tanaka K (1994) Cloning and sequence analysis of cDNA encoding rice glutaredoxin. FEBS Lett 337:157-160 https://doi.org/10.1016/0014-5793(94)80264-5
  36. MOller IM, Liden AC, Ericson I, Gardestrom P (1987) Isolation of submitochondrial particles with different polarities. Methods Enzymol 148:442-453 https://doi.org/10.1016/0076-6879(87)48043-9
  37. Murphy MP (2004) Investigating mitochondrial radical production using targeted probes. Biochem Soc Trans 32:1011-1014 https://doi.org/10.1042/BST0321011
  38. Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125-134 https://doi.org/10.1016/j.tplants.2007.01.005
  39. Nunes-Nesi A, Sweetlove LJ, Fernie AP (2007) Operation and function of the tricarboxylic acid cycle in the illuminated leaf. Physiol Plant 129:45-56 https://doi.org/10.1111/j.1399-3054.2006.00778.x
  40. Park EJ, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen THH (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flower from chilling damage. Plant J 40:474-487 https://doi.org/10.1111/j.1365-313X.2004.02237.x
  41. Pinelli P, Loreto F (2003) $^{12}CO_{2}$ emission from different metabolic pathways measured in illuminated and darkened $C_{3}$ and $C_{4}$ leaves at low, atmospheric, and elevated $CO_{2}$ concentration. J Exp Bot 54:1761-1769 https://doi.org/10.1093/jxb/erg187
  42. Planchet E, Gupta KG, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732-743 https://doi.org/10.1111/j.1365-313X.2005.02335.x
  43. Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546-553 https://doi.org/10.1016/j.tplants.2003.09.015
  44. Rasmusson AG, MOller IM (1991) NAD(P)H dehydrogeneases on the inner surface of the inner mitochondrial membrane studied using inside-out submitochondrial particles. Physiol Plant 83:357-365 https://doi.org/10.1111/j.1399-3054.1991.tb00106.x
  45. Saika H, Ohtsu K, Hamanaka S, Nakazono M, Tsutsumi N, Hirai A (2002) AOX1c, a novel rice gene for alternative oxidase; comparison with rice AOX1a and AOX1b. Gen Genet Sys 77:31-38 https://doi.org/10.1266/ggs.77.31
  46. Santos CVD, Rey R (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:299-334
  47. Sasadadevi K, Raghavendra AS (1992) Dark respiration protects photosynthesis against photoinhibition in mesophyll protoplasts of pea (Pisum sativum). Plant Physiol 99:1232-1237 https://doi.org/10.1104/pp.99.3.1232
  48. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823-826 https://doi.org/10.1038/nature05176
  49. Spalding EP, Goldsmith MHM (1993) Activation of $K^{+}$ channels in the plasma membrane of Arabidopsis by ATP produced photosynthetically. Plant Cell 5:477-484
  50. Stahlberg R, Van Volkenburgh E, Cleland RE (2000) Chlorophyll is not the primary photoreceptor for the stimulation of P-type $K^{+}$pump and growth in variegated leaves of Cleeus X hybridus. Planta 212:1-8 https://doi.org/10.1007/s004250000365
  51. Svensson AS, Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28:73-82 https://doi.org/10.1046/j.1365-313X.2001.01128.x
  52. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891-904 https://doi.org/10.1046/j.1365-313X.2002.01474.x
  53. Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiration metabolism of illuminated leaves. Plant Physiol 138:1596-1606 https://doi.org/10.1104/pp.105.062141
  54. Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: interfaces from the rice genome. J Mol Evol 59:761-770 https://doi.org/10.1007/s00239-004-2666-z
  55. Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physol 128:1271-1281 https://doi.org/10.1104/pp.010999
  56. Tovar-Mendez A, Miernyk JA, Randall DD (2004) Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 270:1043-1049
  57. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C,Seidlitz HK, Zabeau M, Van Montagu M, Inze D, VanBreusegem F (2004) Catalase deficiency drastically affects gene expressioninduced by high light in Arabidopsis thaliana. Plant J 39:45-58 https://doi.org/10.1111/j.1365-313X.2004.02105.x
  58. Villar R, Held AA, Merino J (1995) Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiol 107:421-427
  59. Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447-1456 https://doi.org/10.1104/pp.103.036384
  60. Yoshida K, Noguchi K (2009) Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant Cell Physiol 50:1449-1462 https://doi.org/10.1093/pcp/pcp090
  61. Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092-1111 https://doi.org/10.1093/pcp/pcn086
  62. Zhang L, Li Y, Xing D, Gao C (2009) Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis. J Exp Bot 60:2073-2091 https://doi.org/10.1093/jxb/erp078

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