Skip to main content
Log in

Integrative response of plant mitochondrial electron transport chain to nitrogen source

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Nitrogen (N) availability is widely known as a determinant of plant growth and respiration rate. However, less attention has been paid to the effect of the type of N source (nitrate, nitrite or ammonium) on the respiratory system. This review summarizes the latest findings on this topic, with an emphasis on the effect of ammonium and nitric oxide (NO) on the respiratory system, and the physiological role of alternative oxidase (AOX). First, concentrated ammonium has been found to increase plant respiration rate (ammonium-dependent respiratory increase, ARI). We will introduce two hypotheses to explain ARI, futile ammonium cycling and excess reducing equivalents, and verify the validity of each hypothesis. We suggest that these two hypotheses are not necessarily mutually exclusive. Second, gene expression of AOX is suppressed when N is predominately available as nitrate instead of ammonium. We will discuss possible signaling pathways leading to this expression pattern. Third, while AOX expression is induced by NO, AOX activity itself is insensitive to NO. In contrast, activity of cytochrome c oxidase (COX) is sensitive to NO. We outline the NO production pathway, focusing on nitrite-dependent NO production, and discuss the physiological significance of the fact that AOX activity is insensitive to NO. Finally, this review aims to build an integrated scheme of the respiratory response to the type of N source, considering leaves in high light conditions or hypoxic roots.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    PubMed  CAS  Google Scholar 

  • Atkinson LJ, Hellicar MA, Fitter AH, Atkin OK (2007) Impact of temperature on the relationship between respiration and nitrogen concentration in roots: an analysis of scaling relationships, Q10 values and thermal acclimation ratios. New Phytol 173:110–120

    PubMed  CAS  Google Scholar 

  • Barnard R, Leadley PW (2005) Global change, nitrification, and denitrification: a review. Global Biogeochem Cycles 19:GB1007. doi:10.1029/2004GB002282

  • Barneix AJ, Breteler H, van de Geijn SC (1984) Gas and ion exchanges in wheat roots after nitrogen supply. Physiol Plant 61:357–362

    CAS  Google Scholar 

  • Barth C, Gouzd ZA, Steele HP, Imperio RM (2010) A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. J Exp Bot 61:379–394

    PubMed  CAS  Google Scholar 

  • Becker TW, Foyer C, Caboche M (1992) Light-regulated expression of the nitrate-reductase and nitrite-reductase genes in tomato and in the phytochrome-deficient aurea mutant of tomato. Planta 188:39–47

    CAS  Google Scholar 

  • Beevers L, Hageman RH (1969) Nitrate reduction in higher plants. Annu Rev Plant Biol 20:495–522

    CAS  Google Scholar 

  • Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel M-H, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777:1268–1275

    PubMed  CAS  Google Scholar 

  • Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341

    PubMed  CAS  Google Scholar 

  • Bloom AJ (2002) Assimilation of mineral nutrients. In: Taiz L, Zeiger E (eds) Plant physiology, 3rd edn. Sinauer Associates, Sunderland, pp 259–282

    Google Scholar 

  • Bloom AJ (2009) As carbon dioxide rises, food quality will decline without careful nitrogen management. Calif Agric 63:67–72

    Google Scholar 

  • Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by Barley. Plant Physiol 99:1294–1301

    PubMed  CAS  Google Scholar 

  • Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903

    PubMed  CAS  Google Scholar 

  • Botrel A, Kaiser WM (1997) Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201:496–501

    PubMed  CAS  Google Scholar 

  • Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44:314–333

    PubMed  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant Cell Environ 28:1396–1409

    CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258

    PubMed  CAS  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2002) Subcellular NH4 + flux analysis in leaf segments of wheat (Triticum aestivum). New Phytol 155:373–380

    CAS  Google Scholar 

  • Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Loureiro ME, Fernie AR (2003) Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol 133:1322–1335

    PubMed  CAS  Google Scholar 

  • Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435

    PubMed  CAS  Google Scholar 

  • Clifton R, Lister R, Parker KL, Sappl PG, Elhafez D, Millar AH, Day DA, Whelan J (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol Biol 58:193–212

    PubMed  CAS  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478

    PubMed  CAS  Google Scholar 

  • Curi GC, Welchen E, Chan RL, Gonzalez DH (2003) Nuclear and mitochondrial genes encoding cytochrome c oxidase subunits respond differently to the same metabolic factors. Plant Physiol Biochem 41:689–693

    CAS  Google Scholar 

  • de Graaf MCC, Bobbink R, Roelofs JGM, Verbeek PJM (1998) Differential effects of ammonium and nitrate on three heathland species. Plant Ecol 135:185–196

    Google Scholar 

  • Deng M, Moureaux T, Caboche M (1989) Tungstate, an molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol 91:304–309

    PubMed  CAS  Google Scholar 

  • Dunn AK, Karr EA, Wang Y, Batton AR, Ruby EG, Stabb EV (2010) The alternative oxidase (AOX) gene in Vibrio fischeri is controlled by NrR and upregulated in response to nitric oxide. Mol Microbiol. doi:10.1111/j.1365-2958.2010.07194.x

  • Escobar MA, Geisler DA, Rasmusson AG (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J 45:775–788

    PubMed  CAS  Google Scholar 

  • Frechilla S, Lasa B, Aleu M, Juanarena N, Lamsfus C, Aparicio-Tejo PM (2002) Short-term ammonium supply stimulates glutamate dehydrogenase activity and alternative pathway respiration in roots of pea plants. J Plant Physiol 159:811–818

    CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson P-I, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot J-P (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101:14545–14550

    PubMed  CAS  Google Scholar 

  • Giraud E, van Aken O, Ho LHM, Whelan J (2009) The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of Alternative oxidase1a. Plant Physiol 150:1286–1296

    PubMed  CAS  Google Scholar 

  • Goda H et al (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55:526–542

    PubMed  CAS  Google Scholar 

  • Good AG, Muench DG (1993) Long-term anaerobic metabolism in root tissue. Plant Physiol 101:1163–1168

    PubMed  CAS  Google Scholar 

  • Gray GR, Maxwell DP, Villarimo AR, McIntosh L (2004) Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Rep 23:497–503

    PubMed  CAS  Google Scholar 

  • Guo F-Q, Young J, Crawford NM (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117

    PubMed  CAS  Google Scholar 

  • Guo S, Schinner K, Sattelmacher B, Hansen U-P (2005) Different apparent CO2 compensation points in nitrate- and ammonium-grown Phaseolus vulgaris and the relationship to non-photorespiratory CO2 evolution. Physiol Plant 123:288–301

    CAS  Google Scholar 

  • Gupta KJ, Stoimenova M, Kaiser WM (2005) In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J Exp Bot 56:2601–2609

    PubMed  CAS  Google Scholar 

  • Gupta KJ, Zabalza A, van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391

    PubMed  CAS  Google Scholar 

  • Hachiya T, Terashima I, Noguchi K (2007) Increase in respiratory cost at high growth temperature is attributed to high protein turnover cost in Petunia x hybrida petals. Plant Cell Environ 30:1269–1283

    PubMed  CAS  Google Scholar 

  • Hachiya T, Watanabe CK, Boom C, Tholen D, Takahara K, Kawai-Yamada M, Uchimiya H, Uesono Y, Terashima I, Noguchi K (2010) Ammonium-dependent respiratory increase is dependent on the cytochrome pathway in Arabidopsis thaliana shoots. Plant Cell Environ. doi:10.1111/j.1365-3040.2010.02189.x

  • Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    PubMed  CAS  Google Scholar 

  • Hu H-C, Wang Y-Y, Tsay Y-F (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278

    PubMed  CAS  Google Scholar 

  • Huang X, von Rad U, Dumer J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923

    PubMed  CAS  Google Scholar 

  • Huber JL, Huber SC, Campbell WH, Redinbaugh MG (1992) Reversible light/dark modulation of spinach leaf nitrate reductase activity involves protein phosphorylation. Arch Biochem Biophys 296:58–65

    PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482

    PubMed  CAS  Google Scholar 

  • Kaiser WM, Brendle-Behnisch E (1991) Rapid modulation of spinach leaf nitrate reductase activity by photosynthesis. I. Modulation in vivo by CO2 availability. Plant Physiol 96:363–367

    PubMed  CAS  Google Scholar 

  • Kaiser WM, Brendle-Behnisch E (1995) Acid-base-modulation of nitrate reductase in leaf tissues. Planta 196:1–6

    CAS  Google Scholar 

  • Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989

    PubMed  CAS  Google Scholar 

  • Kim J-H, Guo X, Park H-S (2008) Comparison study of the effects of temperature and free ammonia concentration on nitrification and nitrite accumulation. Process Biochem 43:154–160

    CAS  Google Scholar 

  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494

    PubMed  CAS  Google Scholar 

  • Kronzucker HJ, Britto DT, Davenport R, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337

    PubMed  CAS  Google Scholar 

  • Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246

    PubMed  CAS  Google Scholar 

  • Lager IDA, Andreasson O, Dunbar TL, Andreasson E, Escobar MA, Rasmusson AG (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant Cell Environ. doi:10.1111/j.1365-3040.2010.02161.x

  • Lang B, Kaiser WM (1994) Solute content and energy status of roots of barley plants cultivated at different pH on nitrate- or ammonium-nitrogen. New Phytol 128:451–459

    Google Scholar 

  • Lasa B, Frechilla S, Aparicio-Tejo PM, Lamsfus C (2002) Alternative pathway respiration is associated with ammonium ion sensitivity in spinach and pea plants. Plant Growth Regul 37:49–55

    CAS  Google Scholar 

  • Leakey ADB, Xu F, Gillespie KM, McGrath JM, Ainsworth EA, Ort DR (2009) Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proc Natl Acad Sci USA 106:3597–3602

    PubMed  CAS  Google Scholar 

  • Li Q, Li B-H, Kronzucker HJ, Shi W-M (2010) Root growth inhibition by NH4 + in Arabidopsis is mediated by the root tip and is linked to NH4 + efflux and GMPase activity. Plant Cell Environ. doi:10.1111/j.1365-3040.2010.02162.x

  • Melzer JM, Kleinhofs A, Warner RL (1989) Nitrate reductase regulation: effects of nitrate and light on nitrate reductase mRNA accumulation. Mol Gen Genet 217:341–346

    CAS  Google Scholar 

  • Michalecka AM, Svensson ÅS, Johansson FI, Agius SC, Johanson U, Brennicle A, Binder S, Rasmusson AG (2003) Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol 133:642–652

    PubMed  CAS  Google Scholar 

  • Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398:155–158

    PubMed  CAS  Google Scholar 

  • Millar AH, Hoefnagel MHN, Day DA, Wiskich JT (1996) Specificity of the organic acid activation of alternative oxidase in plant mitochondria. Plant Physiol 111:613–618

    PubMed  CAS  Google Scholar 

  • Miller AJ, Cramer MD (2004) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36

    Google Scholar 

  • Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138

    PubMed  CAS  Google Scholar 

  • Modolo LV, Augusto O, Almeida IMG, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820

    PubMed  CAS  Google Scholar 

  • Møller IM, Rasmusson AG, Fredlund KM (1993) NAD(P)H-ubiquinone oxidoreductases in plant mitochondria. J Bioenerg Biomembr 25:377–384

    PubMed  Google Scholar 

  • Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants––where do we stand? Physiol Plant 138:372–383

    PubMed  CAS  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    PubMed  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) A re-evaluation of the ATP:NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 49:1895–1908

    CAS  Google Scholar 

  • Noguchi K, Terashima I (2006) Responses of spinach leaf mitochondria to low N availability. Plant Cell Environ 29:710–719

    PubMed  CAS  Google Scholar 

  • Oliver SN, Lunn JE, Urbanczyk-Wochniak E, Lytovchenko A, van Dongen JT, Faix B, Schmälzlin E, Fernie AR, Geigenberger P (2008) Decreased expression of cytosolic pyruvate kinase in potato tubers leads to a decline in pyruvate resulting in an in vivo repression of the alternative oxidase. Plant Physiol 148:1640–1654

    PubMed  CAS  Google Scholar 

  • Patrick WH, Reddy KR Jr (1976) Nitrification-denitrification reactions in flooded soils and water bottoms: dependence on oxygen supply and ammonium diffusion. J Environ Qual 5:469–472

    CAS  Google Scholar 

  • Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ. doi:10.1111/j.1365-3040.2010.02158.x

  • Paulissen MPC, van der Ven PJM, Dees AJ, Bobbink R (2004) Differential effects of nitrate and ammonium on three fen bryophyte species in relation to pollutant nitrogen input. New Phytol 164:451–458

    Google Scholar 

  • Planchet E, Gupta KJ, 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

    PubMed  CAS  Google Scholar 

  • Qin C, Qian W, Wang W, Wu Y, Yu C, Jiang X, Wang D, Wu P (2008) GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:18308–18313

    PubMed  CAS  Google Scholar 

  • Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci USA 101:11506–11510

    PubMed  CAS  Google Scholar 

  • Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3-induced stimulation of leaf growth. J Exp Bot 56:1143–1152

    PubMed  CAS  Google Scholar 

  • Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 55:23–39

    PubMed  CAS  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    PubMed  CAS  Google Scholar 

  • Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006a) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925

    PubMed  CAS  Google Scholar 

  • Reich PB, Tjoelker MG, Machado J-L, Oleksyn J (2006b) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439:457–461

    PubMed  CAS  Google Scholar 

  • Rhoads DM, Umbach AL, Sweet CR, Lennon AM, Rauch GS, Siedow JN (1998) Regulation of the cyanide-resistant alternative oxidase of plant mitochondria. J Biol Chem 273:30750–30756

    PubMed  CAS  Google Scholar 

  • Rigano C, Di Martino Rigano V, Vona V, Carfagna S, Carillo P, Esposito S (1996) Ammonium assimilation by young plants of Hordeum vulgare in light and darkness: effects on respiratory oxygen consumption by roots. New Phytol 132:375–382

    CAS  Google Scholar 

  • Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110

    PubMed  CAS  Google Scholar 

  • Rubin G, Tohge T, Matsuda F, Saito K, Scheible W-R (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21:3567–3584

    PubMed  CAS  Google Scholar 

  • Rümer S, Gupta KJ, Kaiser WM (2009) Plant Cells oxidize hydroxylamines to NO. J Exp Bot 60:2065–2072

    PubMed  Google Scholar 

  • Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trend Plant Sci 11:440–448

    CAS  Google Scholar 

  • Scheible W-R, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    PubMed  CAS  Google Scholar 

  • Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499

    PubMed  CAS  Google Scholar 

  • Scheurwater I, Clarkson DT, Purves JV, Van Rijt G, Saker LR, Welschen R, Lambers H (1999) Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant Soil 215:123–134

    CAS  Google Scholar 

  • Schubert S, Yan F (1997) Nitrate and ammonium nutrition of plants: effects on acid/base balance and adaptation of root cell plasmalemma H+ ATPase. Z Pflanzenernähr Bodenkd 160:275–281

    CAS  Google Scholar 

  • Sieger SM, Kristensen BK, Robson CA, Amirsadeghi S, Eng EWY, Abdel-Mesih A, Møller IM, Vanlerberghe GC (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56:1499–1515

    PubMed  CAS  Google Scholar 

  • Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662

    PubMed  CAS  Google Scholar 

  • Stoimenova M, Libourel IGL, Ratcliffe RG, Kaiser WM (2003) The role of nitrate reduction in the anoxic metabolism of roots II. Anoxic metabolism of tobacco roots with or without nitrate reductase activity. Plant Soil 253:155–167

    CAS  Google Scholar 

  • Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474

    PubMed  CAS  Google Scholar 

  • Szczerba MW, Britto DT, Balkos KD, Kronzucker HJ (2008) Alleviation of repid, futile ammonium cycling at the plasma membrane by potassium reveals K+-sensitive and -insensitive components of NH4 + transport. J Exp Bot 59:303–313

    PubMed  CAS  Google Scholar 

  • Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062

    PubMed  CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    PubMed  CAS  Google Scholar 

  • Vanlerberghe GC, Cvetkovska M, Wang J (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plant 137:392–406

    PubMed  CAS  Google Scholar 

  • Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–2522

    PubMed  CAS  Google Scholar 

  • Wang R, Xing X, Crawford NM (2007) Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiol 145:1735–1745

    PubMed  CAS  Google Scholar 

  • Wang R, Xing X, Wang Y, Tran A, Crawford NM (2009) A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol 151:472–478

    PubMed  CAS  Google Scholar 

  • Watanabe CK, Hachiya T, Terashima I, Noguchi K (2008) The lack of alternative oxidase at low temperature leads to a disruption of the balance in carbon and nitrogen metabolism, and to an up-regulation of antioxidant defense systems in Arabidopsis thaliana leaves. Plant Cell Environ 31:1190–1202

    PubMed  CAS  Google Scholar 

  • Watanabe CK, Hachiya T, Takahara K, Kawai M, Uchimiya H, Uesono Y, Terashima I, Noguchi K (2010) Effects of AOX1a deficiency on plant growth, gene expression of respiratory components and metabolic profile under low-nitrogen stress in Arabidopsis thaliana plants. Plant Cell Physiol 51:810–822

    PubMed  CAS  Google Scholar 

  • Welchen E, Chan RL, Gonzalez DH (2002) Metabolic regulation of genes encoding cytochrome c and cytochrome c oxidase subunit Vb in Arabidopsis. Plant Cell Environ 25:1605–1615

    CAS  Google Scholar 

  • Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gene Genet 239:289–297

    CAS  Google Scholar 

  • Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide: insights into regulatory, cytotoxic, adn cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434–456

    PubMed  CAS  Google Scholar 

  • Wright IJ et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    PubMed  CAS  Google Scholar 

  • Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos Trans R Soc London [Biol] 355:1477–1488

    Google Scholar 

  • Yamasaki H (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ 28:78–84

    CAS  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92

    PubMed  CAS  Google Scholar 

  • Yamasaki H, Shimoji H, Ohshiro U, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide 5:261–270

    PubMed  CAS  Google Scholar 

  • Yamaya T, Matsumoto H (1985) Influence of NH4+ on the oxygen uptake of mitochondria isolated from corn and pea shoots. Soil Sci Plant Nutr 31:513–520

    CAS  Google Scholar 

  • Yoshida K, Watanabe CK, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49:592–603

    PubMed  CAS  Google Scholar 

  • Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmälzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098

    PubMed  CAS  Google Scholar 

  • Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428–1440

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. David C. Logan and Dr. D. Tholen for the critical reading of this manuscript. We also thank laboratory members for advice and encouragement. This work is dedicated to Mikiko Hachiya.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takushi Hachiya.

Additional information

Communicated by R. Reski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hachiya, T., Noguchi, K. Integrative response of plant mitochondrial electron transport chain to nitrogen source. Plant Cell Rep 30, 195–204 (2011). https://doi.org/10.1007/s00299-010-0955-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-010-0955-0

Keywords

Navigation