Theoretical and Experimental Plant Physiology

, Volume 28, Issue 4, pp 385–393 | Cite as

The property of progesterone to mitigate cold stress in maize is linked to a modulation of the mitochondrial respiratory pathway

  • Serkan Erdal
  • Mucip GeniselEmail author


Progesterone is associated with growth and development in plants as well as tolerance against environmental stress. However, the molecular mechanisms responsible for the effects of progesterone are not completely understood. In this study, the effects of progesterone on the mitochondrial respiratory pathway (MRP) were investigated in maize seedlings treated with cold stress. Cold stress significantly activated cytochrome pathway (CP) by 61 % and especially alternative respiratory pathway (AP) by 239 % compared with the control, ultimately resulting in an increase by 72 % in the total cellular respiratory rate (TCR). Progesterone alone enhanced CP by 15 %, AP by 59 % and TCR by 15 % compared with control seedlings, whereas the highest values for these parameters were recorded in seedlings subjected to cold plus progesterone. Alternative oxidase (AOX) is the terminal oxidase in the AP. An increase in the AOX gene transcript level was observed in response to cold stress and progesterone, mirroring the increase in AP rate. Meanwhile, AOX protein accumulation exhibited a positive correlation with the AOX gene transcript level. In accordance with the high AP activity, progesterone-treated seedlings exhibited low levels of reactive oxygen species (ROS), including superoxide and hydrogen peroxide, and oxidative damage parameters, including electrolyte leakage and lipid peroxidation levels. Our data demonstrate that the mitigating role of progesterone against the effects of cold stress seems to be linked to the modulation of MRP.


Progesterone in plants Mitochondrial respiration pathway Alternative oxidase Maize Cold 



This work was supported by a grant from the research funds appropriated to Ataturk University, Erzurum, Turkey (2015-354).

Author contributions

M.G. designed and performed most of the experiments. S.E. conceived the idea, designed most of the experiments and supervised the work.


  1. Aydin S, Buyuk I, Aras ES (2014) Expression of SOD gene and evaluating its role in stress tolerance in NaCl and PEG stressed Lycopersicum esculentum. Turk J Bot 38(1):89–98. doi: 10.3906/Bot-1305-1 CrossRefGoogle Scholar
  2. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72(1–2):248–254. doi: 10.1006/abio.1976.9999 CrossRefPubMedGoogle Scholar
  3. Cakmak T, Dumlupinar R, Erdal S (2010) Chilling resistance of Phaseolus vulgaris and Brassica oleracea under a high-intensity electric field. Zeitschrift Fur Naturforschung Section C-a Journal of Biosciences 65(5–6):380–386Google Scholar
  4. Campbell C, Atkinson L, Zaragoza-Castells J, Lundmark M, Atkin O, Hurry V (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytol 176(2):375–389. doi: 10.1111/j.1469-8137.2007.02183.x CrossRefPubMedGoogle Scholar
  5. Chien LF, Wu YC, Chen HP (2011) Mitochondrial energy metabolism in young bamboo rhizomes from Bambusa oldhamii and Phyllostachys edulis during shooting stage. Plant Physiol Biochem 49(4):449–457. doi: 10.1016/j.plaphy.2011.01.024 CrossRefPubMedGoogle Scholar
  6. Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195(1):32–39. doi: 10.1111/j.1469-8137.2012.04166.x CrossRefPubMedGoogle Scholar
  7. Cvetkovska M, Vanlerberghe GC (2013) Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ 36(3):721–732. doi: 10.1111/pce.12009 CrossRefPubMedGoogle Scholar
  8. Dai QS, Shah AA, Garde RV, Yonish BA, Zhang L, Medvitz NA, Miller SE, Hansen EL, Dunn CN, Price TM (2013) A truncated progesterone receptor (PR-M) localizes to the mitochondrion and controls cellular respiration. Mol Endocrinol 27(5):741–753. doi: 10.1210/Me.2012-1292 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Erdal S (2012a) Alleviation of salt stress in wheat seedlings by mammalian sex hormones. J Sci Food Agric 92(7):1411–1416. doi: 10.1002/Jsfa.4716 CrossRefPubMedGoogle Scholar
  10. Erdal S (2012b) Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiol Biochem 57:1–7. doi: 10.1016/j.plaphy.2012.04.016 CrossRefPubMedGoogle Scholar
  11. Erdal S (2012c) Exogenous mammalian sex hormones mitigate inhibition in growth by enhancing antioxidant activity and synthesis reactions in germinating maize seeds under salt stress. J Sci Food Agric 92(4):839–843. doi: 10.1002/Jsfa.4655 CrossRefPubMedGoogle Scholar
  12. Erdal S, Genisel M, Turk H, Gorcek Z (2012) Effects of progesterone application on antioxidant enzyme activities and K +/Na + ratio in bean seeds exposed to salt stress. Toxicol Ind Health 28(10):942–946. doi: 10.1177/0748233711430975 CrossRefPubMedGoogle Scholar
  13. Erdal S, Genisel M, Turk H, Dumlupinar R, Demir Y (2015) Modulation of alternative oxidase to enhance tolerance against cold stress of chickpea by chemical treatments. J Plant Physiol 175:95–101. doi: 10.1016/j.jplph.2014.10.014 CrossRefPubMedGoogle Scholar
  14. Fung RWM, Wang CY, Smith DL, Gross KC, Tian M (2004) MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Sci 166(3):711–719. doi: 10.1016/j.plantsci.2003.11.009 CrossRefGoogle Scholar
  15. Genisel M, Turk H, Erdal S (2013) Exogenous progesterone application protects chickpea seedlings against chilling-induced oxidative stress. Acta Physiol Plant 35(1):241–251. doi: 10.1007/s11738-012-1070-3 CrossRefGoogle Scholar
  16. Gharari Z, Nejad RK, Band RS, Najafi F, Nabiuni M, Irian S (2014) The role of Mn-SOD and Fe-SOD genes in the response to low temperature in chs mutants of Arabidopsis. Turk J Bot 38(1):80–88. doi: 10.3906/Bot-1210-12 CrossRefGoogle Scholar
  17. Grabel’nykh OI, Pobezhimova TP, Pavlovskaya NS, Koroleva NA, Borovik OA, Lyubushkina IV, Voinikov VK (2011) Antioxidant function of alternative oxidase in mitochondria of winter wheat during cold hardening. Biochem (Moscow) Suppl Ser A 5: 249–257Google Scholar
  18. Hanqing F, Kun S, Mingquan L, Hongyu L, Xin L, Yan L, Yifeng W (2010) The expression, function and regulation of mitochondrial alternative oxidase under biotic stresses. Mol Plant Pathol 11(3):429–440. doi: 10.1111/j.1364-3703.2010.00615.x CrossRefPubMedGoogle Scholar
  19. Janeczko A, Filek W (2002) Stimulation of generative development in partly vernalized winter wheat by animal sex hormones. Acta Physiol Plant 24(3):291–295CrossRefGoogle Scholar
  20. Janeczko A, Skoczowski A (2005) Mammalian sex hormones in plants. Folia Histochem Cyto 43(2):71–79Google Scholar
  21. Janeczko A, Oklestkova J, Novak O, Sniegowska-Swierk K, Snaczke Z, Pociecha E (2015) Disturbances in production of progesterone and their implications in plant studies. Steroids 96:153–163. doi: 10.1016/j.steroids.2015.01.025 CrossRefPubMedGoogle Scholar
  22. Karpova OV (2002) Differential expression of alternative oxidase genes in maize Mitochondrial Mutants. The Plant Cell Online 14(12):3271–3284. doi: 10.1105/tpc.005603 CrossRefGoogle Scholar
  23. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227(5259):680. doi: 10.1038/227680a0 CrossRefPubMedGoogle Scholar
  24. Li CR, Liang DD, Xu RF, Li H, Zhang YP, Qin RY, Li L, Wei PC, Yang JB (2013) Overexpression of an alternative oxidase gene, OsAOX1a, improves cold tolerance in Oryza sativa L. Genetics and Molecular Research 12(4):5424–5432. doi: 10.4238/2013.November.11.4 CrossRefPubMedGoogle Scholar
  25. Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl duringdevelopment of rice (Oriza sativa L.) varieties differing in salinity resistance. J Exp Bot 46:1843–1852. doi: 10.1093/jxb/46.12.1843 CrossRefGoogle Scholar
  26. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96(14):8271–8276. doi: 10.1073/pnas.96.14.8271 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Moller IM, Kristensen BK (2004) Protein oxidation in plant mitochondria as a stress indicator. Photochem Photobiol Sci 3(8):730–735. doi: 10.1039/B315561g CrossRefPubMedGoogle Scholar
  28. Mutlu S, Karadagoglu O, Atici O, Tasgin E, Nalbantoglu B (2013) Time-dependent effect of salicylic acid on alleviating cold damage in two barley cultivars differing in cold tolerance. Turk J Bot 37(2):343–349. doi: 10.3906/Bot-1206-17 Google Scholar
  29. Ribas-Carbo M, Aroca R, Gonzalez-Meler MA, Irigoyen JJ, Sanchez-Diaz M (2000) The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol 122(1):199–204. doi: 10.1104/Pp.122.1.199 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Su XY, Wu S, Yang L, Xue RL, Li H, Wang YX, Zhao HJ (2014) Exogenous progesterone alleviates heat and high light stress-induced inactivation of photosystem II in wheat by enhancing antioxidant defense and D1 protein stability. Plant Growth Regul 74(3):311–318. doi: 10.1007/s10725-014-9920-1 CrossRefGoogle Scholar
  31. Sugie A, Naydenov N, Mizuno N, Nakamura C, Takumi S (2006) Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet Syst 81(5):349–354. doi: 10.1266/Ggs.81.349 CrossRefPubMedGoogle Scholar
  32. Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74(2):139–152. doi: 10.1007/s10725-014-9905-0 CrossRefGoogle Scholar
  33. Umbach AL, Lacey EP, Richter SJ (2009) Temperature-sensitive alternative oxidase protein content and its relationship to floral reflectance in natural Plantago lanceolata populations. New Phytol 181(3):662–671. doi: 10.1111/j.1469-8137.2008.02683.x CrossRefPubMedGoogle Scholar
  34. Vanlerberghe GC (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(4):6805–6847. doi: 10.3390/Ijms14046805 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Vanlerberghe GC, McIntosh L (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol 100:115–119CrossRefPubMedPubMedCentralGoogle Scholar
  36. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants—protective role of exogenous polyamines. Plant Sci 151(1):59–66. doi: 10.1016/S0168-9452(99)00197-1 CrossRefGoogle Scholar
  37. Verma KK, Singh M, Gupta RK, Verma CL (2014) Photosynthetic gas exchange, chlorophyll fluorescence, antioxidant enzymes, and growth responses of Jatropha curcas during soil flooding. Turk J Bot 38(1):130–140. doi: 10.3906/Bot-1212-32 CrossRefGoogle Scholar
  38. Wang J, Vanlerberghe GC (2013) A lack of mitochondrial alternative oxidase compromises capacity to recover from severe drought stress. Physiol Plant 149:461–473. doi: 10.1111/ppl.12059 CrossRefPubMedGoogle Scholar
  39. Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z, Bi Y (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol 51(10):1754–1765. doi: 10.1093/pcp/pcq134 CrossRefPubMedGoogle Scholar
  40. Wang J, Rajakulendran N, Amirsadeghi S, Vanlerberghe GC (2011) Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol Plant 142(4):339–351. doi: 10.1111/j.1399-3054.2011.01471.x CrossRefPubMedGoogle Scholar
  41. Yang XH, Xu ZH, Xue HW (2005) Arabidopsis Membrane Steroid Binding Protein 1 is involved in inhibition of cell elongation. Plant Cell 17(1):116–131. doi: 10.1105/tpc.104.028381 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Brazilian Society of Plant Physiology 2016

Authors and Affiliations

  1. 1.Department of Biology, Science FacultyAtaturk UniversityErzurumTurkey
  2. 2.Organic Agriculture Program, Department of Crop and Animal ProductionVocational High SchoolAgriTurkey

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