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Photosynthesis, chilling acclimation and the response of antioxidant enzymes to chilling stress in mulberry seedlings

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Abstract

This study investigates the effects of cold-acclimation in conferring chilling tolerance in seedlings of the mulberry (Morus alba) variety ‘Qiuyu’. Changes in photosynthesis and antioxidant enzymes in chilling acclimatized (CA), and non-acclimatized (NA) seedlings were recorded during chilling stress (3 °C) and a recovery period (25 °C) each for 3 days. The results showed that CA plants had higher net photosynthetic rates (Pn), stomatal conductance (Gs), and maximum photochemical efficiency of photosystem II (Fv/Fm) in response to chilling stress compared to NA. The seedlings maintained the same trends during the recovery stage. The responses of QA reduction degree \((1 - {\text{q}}_{\text{P}} )\) and prime electronic transfer rates (Fo) were lower in acclimatized than in non-acclimatized seedlings. Low-temperature acclimation and chilling stress also caused an increase in leaf proline and soluble sugar contents. Leaf malondialdehyde levels were significantly lower while ascorbate peroxidase (APX) activity was significantly higher in acclimatized seedlings, suggesting that elevated osmolytes and APX confer resistance to chilling temperatures. In this study on the response of mulberry seedlings to chilling stress, we also looked at the recovery process. The response to chilling determines whether mulberry leaves can survive under cold temperatures, while the recovery process determines whether photosynthesis can recover as soon as possible to avoid any secondary damage.

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References

  • Alboresi A, Ballottari M, Hienerwadel R, Giacometti GM, Morosinotto T (2009) Antenna complexes protect photosystem I from photoinhibition. BMC Plant Biol 9(1):71

    PubMed  PubMed Central  Google Scholar 

  • Allen DJ, Ort DR (2000) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Google Scholar 

  • Capell B, Dorffling K (2006) Genotype-specific differences in chilling tolerance of maize in relation to chilling-induced changes in water status and abscisic acid accumulation. Physiol Plant 88:638–646

    Google Scholar 

  • Feng Z, Guo A (2003) Amelioration of chilling stress by triadimefon in cucumber seedlings. Plant Growth Regul 39(3):277–283

    CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    CAS  Google Scholar 

  • Hidekazu S, Ichimura K, Oda M (1996) Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Ann Bot 78:365–369

    Google Scholar 

  • Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of plants to low temperature. Plant Physiol 98:1105–1114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010) The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res 103:175–182

    CAS  PubMed  Google Scholar 

  • Hurry VM, Huner NP (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol 100:1283–1290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jahnke LS, Hull MP, Long SP (1991) Chilling stress and oxygen metabolizing enzymes in Zea diploperennis. Plant, Cell Environ 14:97–104

    CAS  Google Scholar 

  • Janda T, Majláth I, Szalai G (2013) Interaction of temperature and light in the development of freezing tolerance in plants. J Plant Growth Regul 33:460–469

    Google Scholar 

  • John E, Winge P, Bones A (2007) ROS signaling pathways in chilling stress. Plant Signal Behav 5:365–367

    Google Scholar 

  • Jung S, Steffen KL, Lee HJ (1998) Comparative photoinhibition of a high and a low altitude ecotype of tomato (Lycopersicon hirsutum) to chilling stress under high and low light conditions. Plant Sci 134:69–77

    CAS  Google Scholar 

  • Kim YH, Kim MD, Park SC, Yang KS, Jeong JC, Lee HS, Kwak SS (2011) SCOF-1- expressing transgenic sweet potato plants show enhanced tolerance to low-temperature stress. Plant Physiol Biochem 49:1436–1444

    CAS  PubMed  Google Scholar 

  • Klimov SV (2009) Freezing tolerance of winter wheat plants depends on adaptation of photosynthesis and respiration in different time intervals. Biol Bull 36:259–266

    CAS  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant, Cell Environ 23:337–350

    CAS  Google Scholar 

  • Kubota C, Seiyama S, Kozai T (2002) Manipulation of photoperiod and light intensity in low-temperature storage of eggplant plug seedlings. Sci Hortic 94(1):13–20

    Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Annu Rev Plants Physiol 24:445–466

    CAS  Google Scholar 

  • Mishra NP, Mishra RK, Singhal GS (1993) Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol 102:903–910

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2011) Non photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566

    Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Prasad TK (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance: changes in antioxidant system, oxidation of proteins and lipids and protease activities. Plant J 10:1017–1026

    CAS  Google Scholar 

  • Prasad TK, Erson MD, Martin BA, Stewart CR (1994) Evidence for chilling induced oxidative stress in maize seedlings and a regulating role for hydrogen peroxidase. Plant Cell 6:65–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saruyama H, Tanida M (1995) Effect of chilling on activated oxygen-scavenging enzymes in low temperature sensitive and tolerant cultivars of rice (Oryza sativa L.). Plant Sci 109:105–113

    CAS  Google Scholar 

  • Scandalios GJ (1993) Oxygen stress and superoxide dismutase. Plant Physiol 101:7–12

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma P, Sharma N, Deswall R (2005) The molecular biology of the low-temperature response in plants. BioEssays 27:1048–1059

    CAS  PubMed  Google Scholar 

  • Singsaas EL, Ort DR, DeLucia RH (2000) Diurnal regulation of photosynthesis in understory saplings. New Phytol 145:39–49

    Google Scholar 

  • Spichalla JP, Desborogh SL (1990) Superoxide dismutase, catalase, and α-tocopherol content of stored potato tubers. Plant Physiol 94:1214–1218

    Google Scholar 

  • Taranishi Y, Tanaka A, Osumi Fukui S (1974) Catalase activity of hydrocarbon utilizing Candida yeast. Agric Biol Chem 38:1213–1216

    Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    CAS  Google Scholar 

  • Troll W, Lindsey J (1955) A photometric method for the determination of proline. J Bio Chem 215:655–660

    CAS  Google Scholar 

  • Walker MA, Mckersie BD, Pauls KP (1991) Effects of chilling on the biochemical and functional properties of thylakoid membranes. Plant Physiol 97:663–669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JK, Yang DM, Yang YL (1993) Cold resistant mulberry varieties cultivate. Sci Silkworm 19:1–5

    CAS  Google Scholar 

  • Wang JK, Ren SW, Wang DF (2004) Mulberry germ resources in Heilongjiang Province. Science of Silkworm 30(1):73–74

    CAS  Google Scholar 

  • Wise RR, Naylor AW (1987) The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiol 83:272–277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright M, Simon EW (1973) Chilling injury in cucumber leaves. J Exp Bot 24:400–411

    CAS  Google Scholar 

  • Xin ZG, Li PH (1993) Relationship between proline and ABA in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 03:607–613

    Google Scholar 

  • Yong IK, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117

    Google Scholar 

  • Yoshida S, Matsuua C, Etani S (1989) Impairment of tonoplast H-ATPase as an initial physiological response of cells to chilling in mung bean (Vigna radiate [L.] Wilczek). Plant Physiol 89:634–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102

    Google Scholar 

  • Zhan YD, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570

    Google Scholar 

  • Zhang GW, Liu ZL, Zhou JG, Zhu YL (2008) Effects of Ca(NO3)2 stress on oxidative damage, antioxidant enzymes activities and polyamine contents in roots of grafted and non-grafted tomato plants. Plant Growth Regul 56(1):7–19

    CAS  Google Scholar 

  • Zhang ZS, Jia YJ, Gao HY, Zhang LT, Li HD, Meng QW (2011) Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. Planta 234:883–889

    CAS  PubMed  Google Scholar 

  • Zhang ZS, Li G, Gao HY, Zhang LT, Yang C, Liu P, Meng QW (2012) Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence, Zea mays, L. inbred lines. Plos ONE 7(8):e42936

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Bio 10:290–295

    CAS  Google Scholar 

  • Zou Q (2000) Experimental instructions of plant physiology. Agricultural Press, Beijing, pp 110–111

    Google Scholar 

Download references

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Author notes

  1. Xiaojia Liu and Nan Xu have contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Jilin Agricultural University, Changchun, 130118, People’s Republic of China

    Xiaojia Liu

  2. Natural Resources and Ecology Institute, Heilongjiang Academy of Sciences, Harbin, 150040, People’s Republic of China

    Nan Xu, Yining Wu, Jinbo li & Haixiu Zhong

  3. College of Resources and Environment, Northeast Agricultural University, Harbin, 150030, Heilongjiang Province, People’s Republic of China

    Huihui Zhang

Authors
  1. Xiaojia Liu
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  2. Nan Xu
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  3. Yining Wu
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  4. Jinbo li
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  5. Haixiu Zhong
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  6. Huihui Zhang
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Corresponding authors

Correspondence to Haixiu Zhong or Huihui Zhang.

Additional information

Project funding: This work was financially supported by the National Natural Science Foundation (31500323; 41501583; 31370426).

The online version is available at http://www.springerlink.com

Corresponding editor: Hu Yanbo.

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Liu, X., Xu, N., Wu, Y. et al. Photosynthesis, chilling acclimation and the response of antioxidant enzymes to chilling stress in mulberry seedlings. J. For. Res. 30, 2021–2029 (2019). https://doi.org/10.1007/s11676-018-0811-6

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  • DOI: https://doi.org/10.1007/s11676-018-0811-6

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