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24-Epibrassinoslide enhances plant tolerance to stress from low temperatures and poor light intensities in tomato (Lycopersicon esculentum Mill.)

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Abstract

Brassinosteroids (Brs) are a newly recognized group of active steroidal hormones that occur at low concentrations in all plant parts and one of the active and stable forms is 24-epibrassinolide (EBR). We investigated the effect of EBR on tomato (Lycopersicon esculentum Mill.) and its mechanism when seedlings were exposed to low temperature and poor light stress conditions. Leaves of stress-tolerant ‘Zhongza9’ and stress-sensitive ‘Zhongshu4’ cultivars were pre-treated with spray solutions containing either 0.1 μM EBR or no EBR (control). The plants were then transferred to chambers where they were exposed to low temperatures of 12 °C/6 °C (day/night) under a low light (LL) level of 80 μmol · m−2 · s−1. Exogenous application of EBR significantly increased the antioxidant activity of superoxide dismutase, catalase and peroxidase, and decreased the rate of O2 · − formation and H2O2 and malondialdehyde contents. Additionally, the ATP synthase β subunit content was increased by exogenous hormone application. Based on these results, we conclude that exogenous EBR can elicit synergism between the antioxidant enzyme systems and the ATP synthase β subunit so that scavenging of reactive oxygen species becomes more efficient. These activities enable plants to cope better under combined low temperature and poor light stresses.

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Abbreviations

BRs:

Brassinosteroids

CAT:

Catalase

EBR:

24-Epibrassinolide

H2O2 :

Hydrogen peroxide

MALDI-TOF/TOF MS:

Matrix-assisted laser desorption ionization time-of-flight/time-of-flight mass spectrometry

MDA:

Malondialdehyde

MS/MS:

Tandem mass spectrometry

O2 · − :

Superoxide radical

POD:

Peroxidase

ROS:

Reactive oxygen species

SDS-PAGE:

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis

SOD:

Superoxide dismutase

References

  • Abbas S, Latif HH, Elsherbiny EA (2013) Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pak J Bot 45:1273–1284

    CAS  Google Scholar 

  • Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J Genet Plant Breed 46:27–34

    CAS  Google Scholar 

  • Ahmed NU, Park JI, Jung HJ, Hur Y, Nou IS (2015) Anthocyanin biosynthesis for cold and freezing stress tolerance and desirable color in Brassica rapa. Funct Integr Genomics 15:383–394

    Article  CAS  PubMed  Google Scholar 

  • Archambault A, Strömvik MV (2011) PR-10, defensin and cold dehydrin genes are among those over expressed in Oxytropis (Fabaceae) species adapted to the arctic. Funct Integr Genomics 11:497–505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arora P, Bhardwaj R, Kanwar MK (2010) 24-epibrassinolide induced antioxidative defense system of Brassica juncea L. under Zn metal stress. Physiol Mol Biol Plants 16:285–293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Zhang XA, Shu YG, Yue JC (2010) F0F1-ATPase activity regulated by external links on β subunits. Biochem Biophys Res Commun 391:182–186

    Article  CAS  PubMed  Google Scholar 

  • Divi UK, Krishna P (2010) Overexpression of the brassinosteroid biosynthetic gene AtDWF4 in Arabidopsis seeds overcomes abscisic acid-induced inhibition of germination and increases cold tolerance in transgenic seedlings. J Plant Growth Regul 29:385–393

    Article  CAS  Google Scholar 

  • Farhad MS, Babak AM, Reza ZM, Mir Hassan RS, Afshin T (2011) Response of proline, soluble sugars, photosynthetic pigments and antioxidant enzymes in potato (Solanum tuberosum L.) to different irrigation regimes in greenhouse condition. Aust J Crop Sci 5:55–60

    CAS  Google Scholar 

  • Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biol Plant 58:9–17

    Article  CAS  Google Scholar 

  • Fujii S, Saka H (2001) The promotive effect of brassinolide on lamina joint-cell elongation, germination and seedling growth under low-temperature stress in rice (Oryza sativa L.). Plant Prod Sci 4:210–214

    Article  CAS  Google Scholar 

  • Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD, Steffens GL, Flippen-Anderson JL, Cook JC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217

    Article  CAS  Google Scholar 

  • Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ Exp Bot 69:105–112

    Article  CAS  Google Scholar 

  • Hu WH, Wu Y, Zeng JZ, He L, Zeng QM (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48:537–544

    Article  CAS  Google Scholar 

  • Hu M, Qiu ZH, Zhou P, Xu LF, Zhang JK (2012) Proteomic analysis of ‘Zaosu’ pear (Pyrus bretschneideri Rehd.) and its red skin bud mutation. Proteome Sci 10:51

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Janská A, Aprile A, Zámečník J, Cattivelli L, Ovesná J (2011) Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct Integr Genomics 11:307–325

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang YP, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Chen ZX, Yu JQ (2012) Cellular glutathione redox homeostasis plays an important role in the brassinosteroid induced increase in CO2 assimilation in Cucumis sativus. New Phytol 194:932–943

    Article  CAS  PubMed  Google Scholar 

  • Kang GZ, Li GZ, Zheng BB, Han QX, Wang CY, Zhu YJ, Guo TC (2012) Proteomic analysis on salicylic acid-induced salt tolerance in common wheat seedlings (Triticum aestivum L). Biochim Biophys Acta 1824:1324–1333

    Article  CAS  PubMed  Google Scholar 

  • Khalifa NS (2012) Protein expression after NaCl treatment in two tomato cultivars differing in salt tolerance. Acta Biol Cracov 54:79–86

    Google Scholar 

  • Kumar S, Sirhindi G, Bhardwaj R, Kumar M, Arora P (2012) Role of 24-epibrassinolide in amelioration of high temperature stress through antioxidant defense system in Brassica juncea L. Plant Stress 6:55–58

    Google Scholar 

  • Ogweno JO, Song XS, Hu WH, Shi K, Zhou YH, Yu JQ (2009) Detached leaves of tomato differ in their photosynthetic physiological response to moderate high and low temperature stress. Sci Hortic 123:17–22

    Article  CAS  Google Scholar 

  • Rott M, Martins NF, Thiele W, Lein W, Bock R, Kramer DM (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. Plant Cell 23:304–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288

    Article  CAS  PubMed  Google Scholar 

  • Singh I, Kumar U, Singh SK, Gupta C, Singh M, Kushwaha SR (2012) Physiological and biochemical effect of 24-epibrassinoslide on cold tolerance in maize seedlings. Physiol Mol Biol Plants 18:229–236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vardhini BV (2012) Effect of brassinolide on certain enzymes of sorghum grown in saline soils of Karaikal. J Phytol 4:30–33

    Google Scholar 

  • Vardhini BV, Sujatha E, Rao SSR (2011) Brassinosteroids: alleviation of water stress in certain enzymes of sorghum seedlings. J Phytol 3:38–43

    Google Scholar 

  • Wang M, Jiang WJ, Yu HJ (2010) Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato (Lycopersicon esculentum Mill) seedlings under weak light stress. J Agric Food Chem 58:3642–3645

    Article  CAS  PubMed  Google Scholar 

  • Wen L, Tan TL, Shu JB, Chen Y, Liu Y, Yang ZF, Zhang QP, Yin MZ, Tao J, Guan CY (2013) Using proteomic analysis to find the proteins involved in resistance against Sclerotinia sclerotiorum in adult Brassica napus. Eur J Plant Pathol 137:505–523

    Article  CAS  Google Scholar 

  • Wu XX, Yao XF, Chen JL (2014a) Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol Plant 36:251–261

    Article  CAS  Google Scholar 

  • Wu XX, He J, Zhu ZW, Yang SJ, Zha DS (2014b) Protection of photosynthesis and antioxidative system by 24-epibrassinolide in Solanum melongena under cold stress. Biol Plant 58:185–188

    Article  CAS  Google Scholar 

  • Xi ZM, Wang ZZ, Fang YL, Hu ZY, Hu Y, Deng MM, Zhang ZW (2013) Effects of 24-epibrassinolide on antioxidation defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regul 71:57–65

    Article  CAS  Google Scholar 

  • Ye JX, Wang SP, Zhang FJ, Xie DQ, Yao YH (2013) Proteomic analysis of leaves of different wheat genotypes subjected to PEG 6000 stress and rewatering. Plant Omics J 6:286–294

    CAS  Google Scholar 

  • Zhou YH, Yu JQ, Huang LH, Nogues S (2004) The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant Cell Environ 27:1503–1514

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Key Laboratory of Protected Horticultural Engineering in Northwest, Ministry of Agriculture, PR China; and by the State Key Laboratory of Crop Stress Biology for Arid Areas, NWAFU, P R China, and by the Agriculture Research System in China (No. CARS-25-D-02). We also thank Dr. Fengwang Ma (Northwest A&F University, China) and Priscilla Licht for their assistance in revising this composition.

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Lirong Cui, Zhirong Zou, Jing Zhang, Yanyan Zhao & Fei Yan

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  1. Lirong Cui
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  2. Zhirong Zou
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  3. Jing Zhang
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Correspondence to Zhirong Zou.

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Cui, L., Zou, Z., Zhang, J. et al. 24-Epibrassinoslide enhances plant tolerance to stress from low temperatures and poor light intensities in tomato (Lycopersicon esculentum Mill.). Funct Integr Genomics 16, 29–35 (2016). https://doi.org/10.1007/s10142-015-0464-x

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  • DOI: https://doi.org/10.1007/s10142-015-0464-x

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