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The influence of antimycin A on pigment composition and functional activity of photosynthetic apparatus in Triticum aestivum L. under high temperature

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Photosynthetica

Abstract

The purpose of the current investigation was to evaluate the influence of antimycin A (AA) as an activator of the alternative respiratory pathway (AP) on photosynthetic pigment composition and functional activity of the photosynthetic apparatus of wheat seedlings (Triticum aestivum L.) under exposure to high temperature as well as their acclimation. Our results indicated that a significant decrease (44–74%) of photosynthetic pigment contents was caused by a long-term exposure to high temperature (42°C), while the short-term exposure resulted in 20–46% decline. However, a combined effect of AA and long-term high temperature reduced the total pigment contents by 28–41%. Our results demonstrated that the reduction of the chlorophyll a/b ratio was less significant under the combined effect of AA and high temperature than that under the stressful condition without AA. We observed that short-term and long-term high temperature modified PSII functionality of the first leaves in wheat seedlings, which was manifested by the low maximal quantum yield of PSII photochemistry, maximum fluorescence yield in the dark-adapted state, and by high minimum fluorescence yield in the dark-adapted state. The quantum yield of PSII photochemistry decreased rapidly by 16–24% under the combination of AA and high temperature. Overall, these results suggest that the activation of the alternative pathway, induced by AA, contributed to the stabilization of the photosynthetic apparatus in wheat seedlings under high temperature.

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Abbreviations

AA:

antimycin A

AOX:

alternative oxidase

AP:

alternative pathway

Car:

carotenoids

Chl a(b):

chlorophyll a(b)

DAD:

days of development

ETC:

electron transport chain

F0 :

minimal fluorescence yield of the dark-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

FM:

fresh mass

FQR:

ferredoxin plastoquinone oxidoreductase

Fv :

variable fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

LT:

long-term high temperature

NDH:

NADH-dehydrogenase

PGR:

proton gradient regulation

ROS:

reactive oxygen species

ST:

short-term high temperature

References

  • Akman Z.: Comparison of high temperature tolerance in maize, rice and sorghum seeds by plant growth regulators. — J. Anim. Vet. Adv. 8: 358–361, 2009.

    CAS  Google Scholar 

  • Allakhverdiev S.I., Kreslavski V.D., Klimov V.V. et al.: Heat stress: an overview of molecular responses in photosynthesis. — Photosynth Res. 98: 541–550, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Armond P.A., Schreiber U., Björkman O.: Photosynthetic acclimation to temperature in the desert shrub, Larrea divaricata. — Plant Physiol. 61: 411–415, 1978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf M., Harris P.J.C.: Photosynthesis under stressful environments: An overview. — Photosynthetica 51: 163–190, 2013.

    Article  CAS  Google Scholar 

  • Bartoli C.G., Gomez F., Gergoff G. et al.: Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. — J. Exp. Bot. 56: 1269–1276, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Beneragama C.K., Goto K.: Chlorophyll a:b ratio increases under low-light in “shade-tolerant” Euglena gracilis. — Trop. Agr. Res. 22: 12–25, 2010.

    Google Scholar 

  • Biswal A.K., Pattanayak G.K., Pandey S.S. et al.: Light intensitydependent modulation of chlorophyll b biosynthesis and photosynthesis by overexpression of chlorophyllidae a oxygenase in tobacco. — Plant Physiol. 159: 433–449, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borovik O.A., Grabelnych O.I., Koroleva N.A. et al.: The relationships among an activity of the alternative pathway respiratory flux, a content of carbohydrates and a frostresistance of winter wheat. — J. Stress Physiol. Bioch. 9: 241–250, 2013.

    Google Scholar 

  • Brito G., Sofiatti V., Brandão Z.N. et al.: Non-destructive analysis of photosynthetic pigments in cotton plants. — Acta Sci. Agron. 33: 671–678, 2011.

    CAS  Google Scholar 

  • Camejo D., Jiménez A., Alarcón J.J. et al.: Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. — Funct. Plant Biol. 33: 177–187, 2006.

    Article  CAS  Google Scholar 

  • Camejo D., Rodríguez P., Morales M.A. et al.: High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. — J. Plant Physiol. 162: 281–289, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Crafts-Brandner S.J., Salvucci M.E.: Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. — Plant Physiol. 129: 1773–1780, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui L., Li J., Fan Y. et al.: High temperature effects on photosynthesis, PSII functionality and antioxidant activity of two Festuca arundinacea cultivars with different heat susceptibility. — Bot. Stud. 47: 63–69, 2006.

    Google Scholar 

  • Demmig-Adams B., Adams W.W.: Photoprotection and other responses of plants to high light stress. — Annu. Rev. Plant Phys. 43: 599–626, 1992.

    Article  CAS  Google Scholar 

  • Efeoğlu B., Terzioğlu S.: Photosynthetic responses of two wheat varieties to high temperature. — Eurasia J. Biosci. 3: 97–106, 2009.

    Article  Google Scholar 

  • Fikselová M., Šilhár S., Maraček J., Frančáková H.: Extraction of carot (Daucus carota L.) carotenes under different conditions. — Czech J. Food Sci. 26: 268–271, 2008.

    Google Scholar 

  • Gavrilenko V.F., Zhigalova T.V.: Large Workshop on Photosynthesis. Pp. 256. The Academy, Moscow 2003.

    Google Scholar 

  • Georgieva K., Lichtenthaler H.K.: Photosynthetic response of different pea cultivars to low and high temperature treatments. — Photosynthetica 44: 569–578, 2006.

    Article  CAS  Google Scholar 

  • Gilliland A., Singh D.P., Hayward J.M. et al.: Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobaco mosaic virus. — Plant Physiol. 132: 1518–1528, 2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gitelson A.A., Zur Y., Chivkunova O.B., Merzlyak M.N.: Assessing carotenoid content in plant leaves with reflectance spectroscopy. — Photochem. Photobiol. 75: 272–281, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Grabelnych O.I., Borovik O.A., Tauson E.L. et al.: Mitochondrial energy-dissipating systems (alternative oxidase, uncoupling proteins, and external NADH dehydrogenase) are involved in development of frost-resistance of winter wheat seedlings. — Biochemistry-Moscow+ 79: 506–519, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Grabelnych O.I.: The energetic functions of plant mitochondria under stress. — J. Stress Physiol. Bioch. 1: 37–54, 2005.

    Google Scholar 

  • Hasanuzzaman M., Nahar K., Alam M. et al.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. — Int. J. Mol. Sci. 14: 9643–9684, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Havaux M., Ernez M, Lannoye R.: Tolerance of poplar (Populus sp.) to environmental stresses: I. Comparative study of poplar clones using the in vivo chlorophyll fluorescence method. — Acta Oecol. 9: 161–172, 1988.

    Google Scholar 

  • Henriques F.S.: Photosynthetic characteristics of light-sensitive, chlorophyll-deficient leaves from sectorially chimeric stinging-nettle. — Bot. Stud. 49: 235–241, 2008.

    CAS  Google Scholar 

  • Hidema J., Makino A., Mae T., Ojima K.: Photosynthetic characteristics irradiances from full expansion through senescence. — Plant Physiol. 97: 1287–1293, 1991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosler J.P., Yocum C.F.: Evidence for two cyclic photophosphorylation reactions concurrent with ferredoxin-catalyzed noncyclic electron transport. — BBA-Bioenergetics 808: 21–31, 1985.

    Article  CAS  Google Scholar 

  • Huang L., Cobessi D., Tung E.Y., Berry E.A.: Binding of the respiratory chain inhibitor antimycin to the mitochondrial bc1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. — J. Mol. Biol. 351: 573–597, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain I., Wahid A., Rasheed R., Akram H.M.: Seasonal differences in growth, photosynthetic pigments and gas exchange properties in two greenhouse grown maize (Zea mays L.) cultivars. — Acta Bot. Croat. 73: 333–345, 2014.

    CAS  Google Scholar 

  • Joët T., Cournac L., Horvath E. M. et al.: 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. 125: 1919–1929, 2001.

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson G.N.: Physiology of PSI cyclic electron transport in higher plants. — Biochim. Biophys. Acta 1807: 384–389, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Kadir S.: Thermostability of photosynthesis of Vitis aestivalis and V. vinifera. — J. Am. Soc. Hortic. Sci. 131: 476–483, 2006.

    Google Scholar 

  • Kadir S., von Weihe M.: Photochemical efficiency and recovery of photosystem II in grapes after exposure to sudden and gradual heat stress. — J. Am. Soc. Hortic. Sci. 132: 764–769, 2007.

    Google Scholar 

  • Kura-Hotta M., Satoh K., Katoh S. Relationship between photosynthesis and chlorophyll content during leaf senescence of rice seedlings. — Plant Cell Physiol. 28: 1321–1329, 1987.

    CAS  Google Scholar 

  • Lefsrud M.G., Kopsell D.A., Kopsell D.E., Curran-Celentano J.: Air temperature affects biomass and carotenoid pigment accumulation in kale and spinach grown in a controlled environment. — HortScience 40: 2026–2030, 2005.

    CAS  Google Scholar 

  • Lichtenthaler H.K., Buschmann C., Knapp M.: How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. — Photosynthetica 43: 379–393, 2005.

    Article  CAS  Google Scholar 

  • Mathur S., Mehta P., Jajoo A.: Effects of dual stress (high salt and high temperature) on the photochemical efficiency of wheat leaves (Triticum aestivum). — Physiol. Mol. Biol. Plants 19:179–188, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Mavi H.S., Tupper G.T.: Agrometeorology: Principles and Applications of Climate Studies in Agriculture. Pp. 43–68. Haworth Press, Inc., New York, London, Oxford 2004.

    Google Scholar 

  • Mishra R.K., Singhal G.S.: Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. — Plant Physiol. 98: 1–6, 1992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montané M.H., Tardy F., Kloppstech K., Havaux M.: Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance. — Plant Physiol. 118: 227–235, 1998.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mummery R.S., Valadon L.R.G.: The effect of antimycin A on carotenogenesis in Verticillium agaricinum. — Planta 109: 353–356, 1973.

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y., Shikanai T.: Cyclic electron transport through photosystem I. — J. Plant Biotech. 22: 361–369, 2005.

    Article  CAS  Google Scholar 

  • Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. — J. Exp. Bot. 64: 3983–3998, 2013.

    Article  CAS  PubMed  Google Scholar 

  • 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. 37: 71–119, 2002.

    Article  CAS  Google Scholar 

  • Rodríguez V.M., Soengas P., Alonso-Villaverde V. et al.: Effect of temperature stress on the early vegetative development of Brassica oleracea L. — BMC Plant Biol. 15: 1–9, 2015.

    Article  Google Scholar 

  • Roy C., Sengupta D.N.: Effect of short term NaCl stress on cultivars of S. lycopersicum: a comparative biochemical approach. — J. Stress Physiol. Bioch. 10: 59–81, 2014.

    Google Scholar 

  • Sarieva G.E., Kenzhebaeva S.S., Lichtenthaler H.K.: Adaptation potential of photosynthesis in wheat cultivars with a capability of leaf rolling under high temperature conditions. — Russ. J. Plant Physl+ 57: 28–36, 2010.

    Article  CAS  Google Scholar 

  • Scheller H.V.: In vitro cyclic electron transport in barley thylakoids follows two independent pathways. — Plant Physiol. 110: 187–194, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharkey T.D.: Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. — Plant Cell Environ. 28: 269–277, 2005.

    Article  CAS  Google Scholar 

  • Sharma P., Jha A.B., Dubey R.S., Pessarakli M.: Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. — J. Bot. 2012: 217037, 2012.

    Google Scholar 

  • Shikanai T.: Cyclic electron transport around photosystem I: genetic approaches. — Annu. Rev. Plant Biol. 58: 199–217, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Song L., Chow W.S., Sun L. et al.: Acclimation of photosystem II to high temperature in two Wedelia species from different geographical origins: implications for biological invasions upon global warming. — J. Exp. Bot. 61: 4087–4096, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Song Y., Chen Q., Ci D. et al.: Effects of high temperature on photosynthesis and related gene expression in poplar. — BMC Plant Biol. 14: 1–20, 2014.

    Article  Google Scholar 

  • Strodkötter J., Padmasree K., Dinakar C. et al.: Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. — Mol. Plant. 2: 284–297, 2009.

    Article  Google Scholar 

  • Tang Y., Wen X., Lu Q. et al.: Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. — Plant Physiol. 143: 629–638, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tóth S.Z., Schansker G., Kissimon J. et al.: Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.)‒J. Plant Physiol. 162:181–194, 2005.

    Article  PubMed  Google Scholar 

  • Tsonev T., Velikova V., Lambreva M., Stefanov D.: Recovery of the photosynthetic apparatus in bean plants after high-and lowtemperature induced photoinhibition. — Bulg. J. Plant Physiol. 25: 45–53, 1999.

    CAS  Google Scholar 

  • Vanlerberghe G.C.: 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, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warner M.E., Fitt W.K., Schmidt G.W.: Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. — P. Natl. Acad. Sci. USA 96: 8007–8012, 1999.

    Article  CAS  Google Scholar 

  • Wise R.R., Olson A.J., Schrader S.M., Sharkey T.D.: Electron transport is the functional limitation of photosynthesis in field grown cotton plants at high temperature. — Plant Cell Environ. 27: 717–724, 2004.

    Article  CAS  Google Scholar 

  • Yoshida K., Terashima I., Noguchi K.: Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. — Plant Cell Physiol. 47: 22–31, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K., Terashima I., Noguchi K.: Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. — Plant Cell Physiol. 48: 606–614, 2007.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Molecular Biology and Genetics, Department of Ecology, Institute of Life Sciences and Technology, Daugavpils University, Daugavpils, Parades Str. 1a, Latvia

    A. Batjuka, N. Škute & A. Petjukevičs

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  1. A. Batjuka
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  2. N. Škute
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  3. A. Petjukevičs
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Batjuka, A., Škute, N. & Petjukevičs, A. The influence of antimycin A on pigment composition and functional activity of photosynthetic apparatus in Triticum aestivum L. under high temperature. Photosynthetica 55, 251–263 (2017). https://doi.org/10.1007/s11099-016-0231-9

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  • DOI: https://doi.org/10.1007/s11099-016-0231-9

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