Advertisement

Regulation of Reactive Oxygen Species Metabolism and Glyoxalase Systems by Exogenous Osmolytes Confers Thermotolerance in Brassica napus

  • Mirza HasanuzzamanEmail author
  • Kamrun Nahar
  • M. Iqbal R. Khan
  • Jubayer Al Mahmud
  • M. Mahabub Alam
  • Masayuki Fujita
Original Article
  • 1 Downloads

Abstract

In the current study, the beneficial role of proline (Pro) and glycinebetaine (GB) in alleviating high temperature (HT) stress was investigated in Brassica napus L. (rapeseed) seedlings. Ten-d-old rapeseed seedlings were treated with and/or without 2 mM Pro and 2 mM GB and exposed to 38/28 °C day/night (16 and 8 h) temperature for 24 and 48 h. Heat stress induced high amount of hydrogen peroxide (H2O2), lipoxygenase (LOX) and malondialdehyde (MDA) level. Exogenous Pro and GB addition in HT-affected plants increased the levels of ascorbate (AsA) and reduced glutathione (GSH) and their redox pool. Exogenous Pro and GB increased functions of AsA-GSH pathways enzymes along with catalase (CAT), glutathione S-transferase (GST) and glutathione peroxidase (GPX) in HT exposed plants. The enhanced antioxidant defense system by supplementation of Pro and GB helped to reduce oxidative stress and photosynthetic pigments damage caused by HT-induced stress. High methylglyoxal (MG) content decreased upon exogenous Pro and GB application along with enhanced activities of glyoxalase I (Gly I) and Gly II enzymes in HT-stressed plants. Applied Pro and GB under HT stress enhanced endogenous Pro level further to prevent excess water loss and also improved relative water content. Thus, Pro- and/or GB-induced regulatory interactions between ROS and MG detoxification systems may be a useful approach for the reversal of HT-induced oxidative stress.

Keywords

Abiotic stress Extreme temperature Methylglyoxal Osmolytes ROS 

Abbreviations

AO

Ascorbate oxidase

APX

Ascorbate peroxidase

AsA

Ascorbate/ascorbic acid

CAT

Catalase

CDNB

1-Chloro-2,4‑dinitrobenzene

DHA

Dehydroascorbate

DHAR

Dehydroascorbate reductase

Gly I

Glyoxalase I

Gly II

Glyoxalase II

GR

Glutathione reductase

GSH

Reduced glutathione

GSSG

Oxidized glutathione

GPX

Glutathione peroxidase

GST

Glutathione S-transferase

LOX

Lipoxygenase

MDA

Malondialdehyde

MDHA

Monodehydroascorbate

MDHAR

MDHA reductase

MG

Methylglyoxal

NTB

2-Nitro-5-thiobenzoic acid

ROS

Reactive oxygen species

RWC

Relative water content

SLG

S-d-Lactoylglutathione

SNP

Sodium nitroprusside

TBA

Thiobarbituric acid

TCA

Trichloroacetic acid

Die Regulierung des Stoffwechsels reaktiver Sauerstoffspezies und der Glyoxalasesysteme durch exogene Osmolyten führt zu einer Wärmetoleranz bei Brassica napus

Zusammenfassung

In der aktuellen Studie wurde die positive Rolle von Prolin (Pro) und Glycinbetain (GB) bei der Linderung von Stress bei hoher Temperatur (HT) bei Brassica napus L. (Raps)-Setzlingen untersucht. Zehn Tage alte Rapssamen-Sämlinge wurden mit und/oder ohne 2 mM Pro und 2 mM GB behandelt und einer Temperatur von 38/28 °C Tag/Nacht (16 und 8 h) für 24 und 48 h ausgesetzt. Die Hitzebelastung induzierte hohe Menge an Wasserstoffperoxid (H2O2), Lipoxygenase (LOX) und Melondialdehyd (MDA). Die Zugabe von Pro und GB in HT-betroffenen Pflanzen erhöhte die Ascorbat (AsA)-Level und reduzierte Glutathion (GSH) und deren Redoxpool. Exogenes Pro und GB erhöhten die Funktionen der Enzyme der AsA-GSH-Stoffwechselwege, wie Katalase (CAT), Glutathion-S-Transferase (GST) und Glutathionperoxidase (GPX) in HT-exponierten Pflanzen. Das verbesserte antioxidative Abwehrsystem durch die Supplementierung von Pro und GB trug dazu bei, oxidativen Stress und photosynthetische Pigmentschäden zu reduzieren, die durch HT-induzierten Stress verursacht wurden. Der hohe Methylglyoxal (MG)-Gehalt sank bei exogener Pro- und GB-Anwendung durch die erhöhten Aktivitäten von Glyoxalase-I- (Gly I) und Gly-II-Enzymen in HT-gestressten Pflanzen. Das applizierte Pro und GB unter HT-Stress erhöhten den endogenen Pro-Wert weiter, um einen übermäßigen Wasserverlust zu verhindern und den relativen Wassergehalt zu verbessern. Pro- und/oder GB-induzierte regulatorische Wechselwirkungen zwischen ROS- und MG-Entgiftungssystemen können daher ein nützlicher Ansatz für die Umkehrung von HT-induziertem oxidativem Stress sein.

Schlüsselwörter

Abiotischer Stress Extreme Temperatur Methylglyoxal Osmolyten ROS 

Notes

Conflict of interest

M. Hasanuzzaman, K. Nahar, M.I.R. Khan, J.A. Mahmud, M.M. Alam and M. Fujita declare that they have no competing interests.

References

  1. Addinsoft (2017) XLSTAT v. 2017.3: Data analysis and statistics software for Microsoft Excel. Addinsoft, ParisGoogle Scholar
  2. Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Misra AN, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase—Representative H2O2-detoxifying haeme enzymes in plants. Environ Sci Pollut Res Int 23:19002–19029CrossRefGoogle Scholar
  3. Arnon DT (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  4. Asthir B (2015) Mechanisms of heat tolerance in crop plants. Biol Plant 59:620–628CrossRefGoogle Scholar
  5. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428CrossRefGoogle Scholar
  6. Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: Scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  9. Doderer A, Kokkelink I, van der Veen S, Valk B, Schram A, Douma A (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 112:97–104CrossRefGoogle Scholar
  10. Elia AC, Galarini R, Taticchi MI, Dörr AJ, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167CrossRefGoogle Scholar
  11. U.S. Environmental Protection Agency (EPA) (2011) A student’s guide to global climate change. www.epa.gov Google Scholar
  12. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  13. Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione reductase and glutathione: A boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212CrossRefGoogle Scholar
  14. Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6:1746–1751CrossRefGoogle Scholar
  15. Harsh A, Sharma YK, Joshi U, Rampuria S, Singh G, Kumar S, Sharma R (2016) Effect of short-term heat stress on total sugars, proline and some antioxidant enzymes in moth bean (Vigna aconitifolia). Ann Agric Sci 61:57–64CrossRefGoogle Scholar
  16. Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596CrossRefGoogle Scholar
  17. Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365CrossRefGoogle Scholar
  18. Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant responses and tolerance to abiotic oxidative stress: Antioxidant defense is a key factor. In: Bandi V, Shanker AK, Shanker C, Mandapakab M (eds) Crop stress and its management: Perspectives and strategies. Springer, Berlin, pp 261–316CrossRefGoogle Scholar
  19. Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684CrossRefGoogle Scholar
  20. Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2014) Modulation of antioxidant machinery and the methylglyoxal detoxification system in selenium-supplemented Brassica napus seedlings confers tolerance to high temperature stress. Biol Trace Elem Res 161:297–307CrossRefGoogle Scholar
  21. Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H, Fujita M (2017) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200CrossRefGoogle Scholar
  22. Heath RL, Packer L (1968) Photo peroxidation in isolated chloroplasts: Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  23. Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272CrossRefGoogle Scholar
  24. Howarth CJ (2005) Genetic improvements of tolerance to high temperature. In: Ashraf M, Harris PJC (eds) Abiotic stresses: Plant resistance through breeding and molecular approaches. Haworth Press Inc, New York, pp 277–300Google Scholar
  25. Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in ascorbate deficient Arabidopsis mutant. J Exp Bot 56:3041–3049CrossRefGoogle Scholar
  26. Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK (2009) Glycinebetine-induced water-stress tolerance in Cod A‑expressing transgenic India rice is associated with up-regulation of several stress responsive genes. Plant Biotechnol J 7:512–526CrossRefGoogle Scholar
  27. Kaur C, Singla-Pareek SL, Sopory SK (2014) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. CRC Crit Rev Plant Sci 33:429–456CrossRefGoogle Scholar
  28. Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiol Mol Biol Plants 17:203–213CrossRefGoogle Scholar
  29. Khan MIR, Khan NA (2014) Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251:1007–1019CrossRefGoogle Scholar
  30. Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374CrossRefGoogle Scholar
  31. Kocsy G, Laurie R, Szalai G, Szilágyi V, Simon SL, Galiba G, de Ronde JA (2005) Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. Physiol Plant 124:227–235CrossRefGoogle Scholar
  32. Kumar V, Yadav SK (2009) Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress in Camellia sinensis (L.) O. Kuntze. Acta Physiol Plant 31:261–269CrossRefGoogle Scholar
  33. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: Challenges and perspectives. Annu Rev Plant Biol 61:443–462CrossRefGoogle Scholar
  34. Molla MR, Ali MR, Hasanuzzaman M, Al-Mamun MH, Ahmed A, Nazim-Ud-Dowla MAN, Rohman MM (2014) Exogenous proline and betaine-induced upregulation of glutathione transferase and glyoxalase I in lentil (Lens culinaris) under drought stress. Not Bot Horti Agrobot 42:73–80Google Scholar
  35. Måkela P, Jokinen K, Kontturi M, Peltonen-Sainio P, Pehu E, Somersalo S (1998) Foliar application of glycine betaine—a novel product from sugarbeet—as an approach to increase tomato yield. Ind Crops Prod 7:139–148CrossRefGoogle Scholar
  36. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54CrossRefGoogle Scholar
  37. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016a) Polyamine and nitric oxide crosstalk: Antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense, and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255CrossRefGoogle Scholar
  38. Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Mahmud JA, Suzuki T, Fujita M (2017) Insights into spermine-induced combined high temperature and drought tolerance in mung bean: Osmoregulation and roles of antioxidant and glyoxalase system. Protoplasma 254:445–460CrossRefGoogle Scholar
  39. Nahar K, Hasanuzzaman M, Fujita M (2016b) Roles of osmolytes in plants adaptation to drought and salinity. In: Iqbal N, Nazar R, Khan NA (eds) Osmolytes and plants acclimation to changing environment: Emerging omics technologies. Springer, New York, pp 37–68CrossRefGoogle Scholar
  40. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  41. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: An integrated overview. Plant Cell Environ 35:454–484CrossRefGoogle Scholar
  42. Oukarroum A, El Madidi S, Strasser RJ (2012) Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): A chlorophyll a fluorescence study. Plant Biosyst 146:1037–1043CrossRefGoogle Scholar
  43. Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140CrossRefGoogle Scholar
  44. Poli Y, Basava RK, Panigrahy M, Vinukonda VP, Dokula NR, Voleti SR, Desiraju S, Neelamraju S (2013) Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits. Rice (N Y) 6:36CrossRefGoogle Scholar
  45. Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of wistar rats. Biochem Biophys Acta 911:349–355Google Scholar
  46. Rasheed R, Wahid A, Farooq M, Hussain I, Basra SMA (2011) Role of proline and glycinebetaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. Plant Growth Regul 65:35–45CrossRefGoogle Scholar
  47. Shin H, Oh S, Arora R, Kim D (2016) Proline accumulation in response to high temperature in winter-acclimated shoots of Prunus persica: A response associated with growth resumption or heat stress? Can J Plant Sci 96:630–638CrossRefGoogle Scholar
  48. Sorwong A, Sakhonwasee S (2015) Foliar application of glycine betaine mitigates the effect of heat stress in three marigold (Tagetes erecta) cultivars. Hortic J 84:161–171CrossRefGoogle Scholar
  49. Suriyasak C, Harano K, Tanamachi K, Matsuo K, Tamada A, Iwaya-Inoue M, Ishibashi Y (2017) Reactive oxygen species induced by heat stress during grain filling of rice (Oryza sativa L.) are involved in occurrence of grain chalkiness. J Plant Physiol 216:52–57CrossRefGoogle Scholar
  50. The Intergovernmental Panel on Climate Change (IPCC) (2014) Climate change and water. In: Bates BC, Kundzewicz ZW, Palutikof J, Wu S (eds) Technical paper of the Intergovernmental Panel for Climate Change. IPCC, Genf, p 210Google Scholar
  51. Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: The N‑acetyl-l-cysteine assay. Anal Bioanal Chem 403:2577–2581CrossRefGoogle Scholar
  52. Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23:51–68CrossRefGoogle Scholar
  53. Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963CrossRefGoogle Scholar
  54. Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2-12Google Scholar

Copyright information

© Springer-Verlag GmbH Deutschland, ein Teil von Springer Nature 2019

Authors and Affiliations

  • Mirza Hasanuzzaman
    • 1
    Email author
  • Kamrun Nahar
    • 2
  • M. Iqbal R. Khan
    • 3
  • Jubayer Al Mahmud
    • 4
  • M. Mahabub Alam
    • 1
  • Masayuki Fujita
    • 5
  1. 1.Department of Agronomy, Faculty of AgricultureSher-e-Bangla Agricultural UniversitySher-e-Bangla Nagar, Dhaka-1207Bangladesh
  2. 2.Department of Agricultural Botany, Faculty of AgricultureSher-e-Bangla Agricultural UniversitySher-e-Bangla Nagar, Dhaka-1207Bangladesh
  3. 3.Plant System Biology Laboratory, Department of BotanyJamia HamdardNew Delhi-110062India
  4. 4.Department of Agroforestry and Environmental ScienceSher-e-Bangla Agricultural UniversitySher-e-Bangla Nagar, Dhaka-1207Bangladesh
  5. 5.Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of AgricultureKagawa UniversityMiki-cho, Kita-gunJapan

Personalised recommendations