Roślinny mitochondrialny łańcuch oddechowy

• Authors: Monika Ostaszewska-Bugajska , Anna Podgórska , Anna Rychter , Bożena Szal

Title variants

EN

Plant mitochondrial respiratory chain

• Languages of publication: PL EN

Abstracts

PL

Roślinny mitochondrialny łańcuch oddechowy, oprócz dużych kompleksów białkowych (Kompleksów I-IV) zawiera dodatkowe elementy: wewnętrzne i zewnętrzne dehydrogenazy typu II (NDin/NDex) utleniające NAD(P)H pochodzące odpowiednio z macierzy mitochondrialnej lub cytozolu oraz dodatkową terminalną oksydazę nazwaną oksydazę alternatywną (AOX). Udział szlaków alternatywnych w oddychaniu musi być ściśle regulowany ponieważ aktywność tych enzymów nie jest związana z translokacją protonów w poprzek błony i w konsekwencji nie prowadzi do produkcji ATP. Aktywność ta pozwala natomiast rozproszyć nadmiar siły redukcyjnej, co jest szczególnie ważne w warunkach stresowych. W tym artykule przeglądowym omówiono budowę szlaków alternatywnych roślinnego mtETC, regulację ich aktywności na różnych poziomach oraz opisano role jakie pełnią NDin/ex i AOX w metabolizmie komórek roślinnych.

EN

Plant mitochondrial electron transport chain (mtETC), besides large complexes (Complex I-IV), consists of additional elements: internal and external type II NAD(P)H dehydrogenases (NDin/NDex) and an additional terminal oxidase, named alternative oxidase (AOX). The engagement of alternative pathways in respiration must be tightly regulated since their activity is not linked to pumping protons across membrane and, as a consequence, is not associated with ATP synthesis. The activity of plant-specific components in mtETC allows to dissipate the excess of reducing power and may be especially important under stress conditions. In this review the structure, the regulation of activities and the role of NDin/NDex and AOX in metabolism of plant cells is described.

Keywords

PL

oksydaza alternatywna; dehydrogenazy typu II; mitochondria roślinne; oddychanie cyjanoodporne; szlaki alternatywne w roślinnym mtETC

• Journal: Kosmos
• Year: 2015
• Volume: 64
• Issue: 3
• Pages: 401-414

Dates

published

2015

Contributors

author

Monika Ostaszewska-Bugajska

• Zakład Anatomii i Cytologii Roślin, Instytut Biologii Eksperymentalnej i Biotechnologii Roślin, Wydział Biologii Uniwersytetu Warszawskiego, Miecznikowa 1, 02-096 Warszawa, Polska

author

Anna Podgórska

• Zakład Anatomii i Cytologii Roślin, Instytut Biologii Eksperymentalnej i Biotechnologii Roślin, Wydział Biologii Uniwersytetu Warszawskiego, Miecznikowa 1, 02-096 Warszawa, Polska

author

Anna Rychter

• Zakład Anatomii i Cytologii Roślin, Instytut Biologii Eksperymentalnej i Biotechnologii Roślin, Wydział Biologii Uniwersytetu Warszawskiego, Miecznikowa 1, 02-096 Warszawa, Polska

author

Bożena Szal

• Zakład Anatomii i Cytologii Roślin, Instytut Biologii Eksperymentalnej i Biotechnologii Roślin, Wydział Biologii Uniwersytetu Warszawskiego, Miecznikowa 1, 02-096 Warszawa, Polska

References

• Arnhold-Schmitt B., Costa J. H., Fernandes de Melo D., 2006. AOX - a functional marker for efficient cell reprograming under stress? Trends Plant Sci. 11, 281-287.
• Carnevali F., De Santis A., 2009. Activity and expression of alternative pathways of respiration during postharvest cold storage of kiwifruit. EMBL/GenBank/DDBJ databases.
• Carrie C., Murcha M. W., Kuehn K., Duncan O., Barthet M., Smith P. M., Eubel H., Meyer E ., Day D. A., Millar A. H., Whelan J., 2008. Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079.
• Clifton R., Lister R., Parker K. L., Sappl P. G., Elhafez D., Millar A. H., Day D. A., Whelan J., 2005. Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193-212.
• Clifton R., Millar A. H., Whelan J., 2006. Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim. Biophys. Acta. 1757, 730-741.
• Considine M. J., Holtzapffel R. C., Day D. A., Whelan J., Millar H., 2002. Molecular distintion between alternative oxidase from monocots and dicots. Plant Physiol. 129, 949-953.
• Costa J. H., McDonald A. E., Arnholdt-Schmitt B., Fernandes de Melo D., 2014. A classification scheme for alternative oxidases reveals the taxonomic distribution and evolutionary history of the enzyme in angiosperms. Mitochondrion 19, 172-183.
• Day D. A, Krab K., Lambers H., Moore A. L., Siedow J. N., Wagner A. M., Wiskich J. T. 1996. The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiol. 110, 1-2.
• Dinakar C., Raghavendra A.S., Padmasree K., 2010. Importance of AOX pathway in optimizing photosynthesis under high light stress: role of pyruvate and malate in activating AOX. Physiol. Plant. 139, 13-26.
• Elhafez D., Murcha M. W., Clifton R., Soole K. L., Day D. A., Whelan J., 2006. Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol. 47, 43-54.
• Escobar M. A., Franklin K. A., Svensson A. S., Salter M. G., Whitelam G. C., Rasmusson A. G., 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.
• Escobar M. A., Geisler D. A., Rasmusson A. G., 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.
• Felle H. H., 2001. pH: signal and messenger in plant cells. Plant Biol. 3, 577-591.
• Feng H., Li H., Li X., Duan J., Liang H., Zhi D., Ma J., 2007. The flexible interrelation between AOX respiratory pathway and photosynthesis in rice leaves. Plant Physiol. Biochem. 45, 228-235.
• Florez-Sarasa I., Ostaszewska M., Galle A., Flexas J., Rychter A. M., Ribas-Carbó M., 2009. Changes of alternative oxidase activity, capacity and protein content in leaves of Cucumis sativus wild-type and MSC16 mutant grown under different light intensities. Physiol. Plant. 137, 419-426.
• Geisler D. A., Broselid C., Hederstedt L., Rasmusson A. G., 2007. Ca2+-binding and Ca2+-independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J. Biol. Chem. 282, 28455-28464.
• Giraud E., Ho L. H., Clifton R., Carroll A ., Estavillo G., Tan Y. F., Howell K. A., Ivanova A., Pogson B. J., Millar A. H., Whelan J., 2008. The absence of alternative oxidase 1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 147, 595-610.
• Gomes C. M., Le Gall J., Xavier A. V., Teixeira M., 2001. Could a diiron-containing four-helix-bundle protein have been a primitive oxygen reductase? ChemBioChem 2, 583-587.
• Gupta K. J., Zabalza A., van Dongen J. T., 2009. Regulation of respiration when the oxygen availability changes. Physiol. Plant. 137, 383-391.
• Guy R. D., Berry J. A., Fogel M. L., Hoering T. C., 1989. Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 177, 483-491.
• Hiser C., Kapranov P., McIntosh L., 1996. Genetic modification of respiratory capacity in potato. Plant Physiol. 110, 277-286.
• Ho L. H., Giraud E., Uggalla V., Lister R., Clifton R., Glen A., Thirkettle-Watts D., Van Aken O., Whelan J., 2008. Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147, 1858-1873.
• Johansson F. I., Michalecka A. M., Mø ller I. M., Rasmusson A. G., 2004. Oxidation and reduction of pyridine nucleotides in alamethicin-permeabilized plant mitochondria. Biochem. J. 380, 193-202.
• Juszczuk I. M., Rychter A. M., 2001. Regulacja aktywności oksydazy alternatywnej. Post. Bioch. 47, 318-327.
• Juszczuk I. M., Rychter A. M., 2003. Alternative oxidase in higher plants. Acta Biochim. Pol. 4, 1257-1271.
• Kerscher S. J., 2000. Diversity and origin of alternative NADH:ubiquinone oxidoreductases. Biochim. Biophys. Acta. 1459, 274-283.
• Lambers H., 1985. Respiration in intact plants and tissues: Its regulation and dependence on environmental factors, metabolism and invaded organisms. [W:] Higher Plant Cell Respiration (Encyclopedia of Plant Physiology, new series, vol. 18). Douce R., Day D. A. (red.). Springer, Berlin, 418-473.
• Liu Y. J., Norberg F. E. B., Szilágyi A., De Paepe R., Åkerlund H. E., Rasmusson A. G., 2008. The mitochondrial external NADPH dehydrogenase modulates the leaf NADPH/NADP+ ratio in transgenic Nicotiana sylvestris. Plant Cell Physiol. 49, 251-263.
• Logan D. C., Knight M. R., 2003. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol. 133, 21-24.
• Maxwell D. P., Wang Y., McIntosh L., 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA. 96, 8271-8276.
• McDonald A. E., Vanlerberghe G. C., Staples J. F., 2009. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 212, 2627-2634.
• Michalecka A. M., Svensson A. S., Johansson F. I., Agius S. C., Johanson U., Brennicke A., Binder S., Rasmusson A. G., 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.
• Michalecka A. M., Agius S. C., Møller I. M., Rasmusson A. G., 2004. Identification of a mitochondrial NADPH dehydrogenase by overexpression in transgenic Nicotiana sylvestris. Plant J. 37, 415-425.
• Millenaar F. F., Lambers H., 2003. The alternative oxidase: in vivo regulation and function. Plant Biol 5, 2-15.
• Møller I. M., 2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561-591.
• Moore A. L., Shiba T., Young L., Harada S., Kita K., Ito K., 2013. Unraveling the heater: new insights into the structure of the alternative oxidase. Annu. Rev. Plant Biol. 64, 637-663.
• Moore C. S., Cook-Johnson R. J., Rudhe C., Whelan J., Day D. A., Wiskich J. T., Soole K. L., 2003. Identification of AtNDI1, an internal nonphosphorylating NAD(P)H dehydrogenase in Arabidopsis thaliana mitochondria. Plant Physiol. 133, 1-11.
• Podgórska A., Gieczewska K., Łukawska-Kuźma K., Rasmusson A. G., Gardeström P., Szal B., 2013. Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)+ ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant Cell Environ. 36, 2034-2045.
• Rasmusson A. G., Møller I. M., 1991. NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial-membrane studied using inside-out submitochondrial particles. Physiol. Plant. 83, 357-365.
• Rasmusson A. G., Møller I. M., 2006. Multiple energy-conservation bypasses in oxidative phosphorylation of plant mitochondria plant physiology. http://4e.plantphys.net/article.php?ch=7&id=350.
• Rasmusson A. G., Svensson A. S., Knoop V., Grohmann L., Brennicke A., 1999. Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J. 20, 79-87.
• Rasmusson A. G., Soole K. L., Elthon T. E., 2004. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 55, 23-39.
• Rasmusson A. G., Geisler D. A., Møller I. M., 2008. The multiplicity of dehydrogenases in the electrontransport chain of plant mitochondria. Mitochondrion 8, 47-60.
• Rasmusson A. G., Fernie A. R., Van Dongen J. T., 2009. Alternative oxidase: a defence against metabolic fluctuations? Physiol. Plant. 137, 371-382.
• Ribas-Carbó M., Robinson S. A., González-Meler M. A., Lennon A. M., Giles L., Siedow J. N., Berry J. A., 2000. Effects of light respiration and oxygen isotope fractionation in soybean cotyledons. Plant Cell Environ. 23, 983-989.
• Ribas-Carbó M., Robinson S.A., Giles L., 2005. The application of the oxygen-isotope techniqe to assess respiratory pathway partitioning. [W:] Plants Respiration: From Cell to Ecosystem. Lambers H., Ribas-Carbó M. (red.). Springer, Berlin, 31-41.
• Robinson S. A., Ribas-Carbó M., Yakir D., Giles L., Reuveni Y., Berry J. A., 1995. Beyond SHAM and cyanide: opportunities for studying the alternative oxidase in plant respiration using oxygen isotope discrimination. Aust. J. Plant Physiol. 22, 487-496.
• Rustin P., Jacobs H. T., 2009. Respiratory chain alternative enzymes as tools to better understand and counteract respiratory chain deficiencies in human cells and animals. Physiol. Plant 137, 362-370.
• Rychter A. M., Chauveau M., Bomsel J. L., Lance C., 1992. The effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots. Physiol. Plant. 84, 80-86.
• Shiba T., Kido Y., Sakamoto K., Inaoka D. K., Tsuge C., Tatsumi R., Takahashi G., Balogun E. O., Nara T., Aoki T., Honma T., Tanaka A., Inoue M., Matsuoka S., Saimoto H., Moore A. L., Harada S., Kita K., 2013. Structure of the trypanosome cyanide-insensitive alternative oxidase. Proc. Nat. Acad. Sci. USA 110, 4580-4585.
• Sieger S. M., Kristensen B. K., Robson C. A., Amirsadeghi S., Eng E. W., Abdel-Mesih A., Møller I. M., Vanlerberghe G. C., 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.
• Smith C., Barthet M., Melino V., Smith P., Day D., Soole K., 2011. Alterations in the mitochondrial alternative NAD(P)H dehydrogenase NDB4 lead to changes in mitochondrial electron transport chain composition, plant growth and response to oxidative stress. Plant Cell Physiol. 52, 1222-1237.
• Svensson A. S., Johansson F. I., Mø ller I. M., Rasmusson A. G., 2002. Cold stress decreases the capacity for respiratory NADH oxidation in potato leaves. FEBS Lett. 517, 79-82.
• Szal B., Podgórska A., 2012. The role of mitochondria in leaf nitrogen metabolism. Plant Cell Environ. 35, 1756-1768.
• Umbach A. L., Fiorani F., Siedow J. N., 2005. Characterization of transformed Arabidopsis with altered oxidase levels and analysis of effect on reactive oxygen species in tissue. Plant Physiol. 139, 1806-1820.
• Vanlerberghe G. C., 2013. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int. J. Mol. Sci. 14, 6805-6847.
• Vanlerberghe G. C., Vanlerberghe A. E., McIntosh L., 1994. Molecular genetic alteration of plant respiration. Silencing and overexpression of alternative oxidase in transgenic tobacco. Plant Physiol. 106, 1503-1510.
• Vanlerberghe G. C., 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.
• Wallström S. V., Florez-Sarasa I., Araújo W. L., Aidemark M., Fernández-Fernández M., Fernie A. R., Ribas-Carbó M., Rasmusson A. G., 2014a. Suppression of the external mitochondrial NADPH dehydrogenase, NDB1, in Arabidopsis thaliana affects central metabolism and vegetative growth. Mol. Plant. 7, 356-368.
• Wallström S. V., Florez-Sarasa I., Araújo W. L., Escobar M. A., Geisler D. A., Aidemark M., Lager I., Fernie A. R., Ribas-Carbó M., Rasmusson A. G., 2014b. Suppression of NDA-type alternative mitochondrial NAD(P)H dehydrogenases in Arabidopsis thaliana modifies growth and metabolism, but not high light stimulation of mitochondrial electron transport. Plant Cell Physiol. 55, 881-896.
• Watanabe C. K., 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 defence systems in Arabidopsis thaliana leaves. Plant Cell Environ. 31, 1190-1202.
• Xu F., Yuan S., Lin H. H., 2011. Response of mitochondrial alternative oxidase (AOX) to light signals. Plant Signal. Behav. 6, 55-58.
• Xu L., Law S. R., Murcha M. W., Whelan J., Carrie C., 2013. The dual targeting ability of type II NAD(P)H dehydrogenases arose early in land plant evolution. BMC Plant Biol. 13, 100.
• Yoshida K., Terashima I., Noguchi K., 2007. Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48, 606-614.
• Zhang D. W., Xu F., Zhang Z. W., Chen Y. E., Du J. B., Jia S. D., Yuan S., Lin H. H., 2010. Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. Plant Cell Environ. 33, 2121-2131.