Skip to main content
SpringerLink
Log in

Role of methylglyoxal and its detoxification system in plant thermotolerance

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

With the development of global warming and greenhouse effect, heat stress (HS) has become a major stress factor affecting cellular metabolism, plant growth, development, productivity, and even survival. Therefore, understanding the mechanisms of heat injury and thermotolerance in plants is important for agricultural and ecological industry. In general, heat injury leads to protein denaturation, biomembrane damage, oxidative stress, osmotic stress, methylglyoxal (MG) stresses, and ion and nutrient imbalance. Correspondingly, MG as signalling molecule can trigger plant thermotolerance, which is implicated in modification of heat shock proteins (HSPs), biomembrane repair, enhancement of antioxidant system, accumulation of osmolytes, stimulation of MG-detoxification system, and biosynthesis of transporters. In this review, based on the current progress in methylglyoxal (MG) as glycating agent and signalling molecule as well as its detoxification system, MG homeostasis in plants, the mechanisms of heat injury induced by MG as glycating agent and thermotolerance triggered by MG as signalling molecule were summarised. The review is designed to further expound the mechanisms of heat injury and thermotolerance in plants, to stir up the rapid development of MG signalling in plant biology. In addition, the paper lays the foundation of acquiring transgenic crop plants with thermotolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ABRE:

ABA response element

AG:

Aminoguanidine

AGE:

Advanced glycation end products

AKR:

Aldo–keto reductase

ALE:

Advanced lipid peroxidation end products

APX:

Ascorbate peroxidase

ARE:

Auxin response element

AsA:

Ascorbic acid

ASA:

Acetylsalicylic acid

AOR:

Aldose/aldehyde reductase

CAR:

Carnosine

CAT:

Catalase

Cur:

Curcumin

ERE:

Ethylene response element

Gly:

Glyoxalase

GR:

Glutathione reductase

GSH:

Glutathione

HSE:

Heat shock element

LDH:

Lactate dehydrogenase

MAPK:

Mitogen-activated protein kinase

MDA:

Malondialdehyde

MG:

Methylglyoxal

MGDH:

Methylglyoxal dehydrogenase

MGR:

Methylglyoxal reductase

MGRE:

Methylglyoxal response element

O2 − :

Superoxide anion radical

PC:

Protein carbonyls

PM:

Pyridoxamine

POD:

Peroxidase

ROS:

Reactive oxygen species

SnRK:

Sucrose non-fermenting related protein kinase

SOD:

Superoxide dismutase

UV:

Ultraviolet

References

  • Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  CAS  PubMed  Google Scholar 

  • Aleem S, Sharif I, Amin E, Tahir M, Parveen N, Aslam R, Najeebullah M, Shahid MTH (2020) Heat tolerance in vegetables in the current genomic era: an overview. Plant Growth Regul 92:497–516

    Article  CAS  Google Scholar 

  • Ali S, Rizwan M, Arif MS, Ahmad R, Hasanuzzaman M, Ali B, Hussain A (2020) Approaches in enhancing thermotolerance in plants: an updated review. J Plant Growth Regul 39:456–480

    Article  CAS  Google Scholar 

  • Asthir B (2015) Mechanisms of heat tolerance in crop plants. Biol Plant 59:620–628

    Article  CAS  Google Scholar 

  • Banerjee A, Tripathi DK, Roychoudhury A (2018) Hydrogen sulphide trapeze: environmental stress amelioration and phytohormone crosstalk. Plant Physiol Biochem 132:46–53

    Article  CAS  PubMed  Google Scholar 

  • Bhowal B, Singla-Pareek SL, Sopory SK, Kaur C (2020) From methylglyoxal to pyruvate: a genome-wide study for the identification of glyoxalases and d-lactate dehydrogenases in Sorghum bicolor. BMC Genom 21:145

    Article  CAS  Google Scholar 

  • Bless Y, Ndlovu L, Gokul A, Keyster M (2017) Exogenous methylglyoxal alleviates zirconium toxicity in Brassica rapa L. seedling shoots. S Afr J Bot 109:327

    Article  Google Scholar 

  • Ding Y, Shi Y, Yang S (2020) Molecular regulation of plant response to environmental temperatures. Mol Plant 13:544–564

    Article  CAS  PubMed  Google Scholar 

  • Dong W (2016) Genome-wide analysis of glyoxalase system and functional identification of zmGLYI-8 gene in maize. Shandong Agricultural University. MA thesis

  • El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    Article  CAS  PubMed  Google Scholar 

  • Fu ZW, Li JH, Feng YR, Yuan X, Lu YT (2021) The metabolite methylglyoxal-mediated gene expression is associated with histone methylglyoxalation. Nucleic Acids Res 49:1886–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garai S, Bhowal B, Pareek A, Singla-Pareek SL, Kaur C, Sopory SK (2021) Expression dynamics of glyoxalase genes under high temperature stress in plants. Plant Physiol Rep 25:533–548

    Article  CAS  Google Scholar 

  • Ghosh A (2017) Genome-wide identification of glyoxalase genes in Medicago truncatula and their expression profiling in response to various developmental and environmental stimuli. Front Plant Sci 8:836

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghosh A, Islam T (2016) Genome-wide analysis and expression profiling of glyoxalase gene families in soybean (Glycine max) indicate their development and abiotic stress specific response. BMC Plant Biol 16:87

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghosh A, Kushwaha H, Hasan MR, Pareek A, Sopory S, Singla-Pareek S (2016) Presence of unique glyoxalase III proteins in plants indicates the existence of shorter route for methylglyoxal detoxification. Sci Rep 6:18358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776

    Article  CAS  PubMed  Google Scholar 

  • Gupta BK, Sahoo KK, Ghosh A, Tripathi AK, Anwar K, Das P, Singh AK, Pareek A, Sopory SK, Singla-Pareek SL (2017) Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant Cell Environ 41:1186–1200

    Article  PubMed  CAS  Google Scholar 

  • 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 14:9643–9684

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 161:297–307

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Khan MIR, Mahmud JA, Alam MM, Fujita M (2020) Regulation of reactive oxygen species metabolism and glyoxalase systems by exogenous osmolytes confers thermotolerance in Brassica napus. Gesunde Pflanzen 72:3–16

    Article  CAS  Google Scholar 

  • Hoque TS, Okuma E, Uraji M, Furuichi T, Sasaki T, Hoque MA, Nakamura Y, Murata Y (2012a) Inhibitory effects of methylglyoxal on light-induced stomatal opening and inward K+ channel activity in Arabidopsis. Biosci Biotechnol Biochem 76:617–619

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Ye W, Hossain MA, Nakamura Y, Murata Y (2012b) Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 169:979–986

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Tuya A, Nakamura Y, Murata Y (2012c) Methylglyoxal inhibits seed germination and root elongation and up-regulates transcription of stress-responsive genes in ABA-dependent pathway in Arabidopsis. Plant Biol 14:854–858

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran L-SP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:872875

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Islam MM, Ye W, Matsushima D, Munemasa S, Okuma F, Nakamura Y, Biswas S, Mano J, Murata Y (2016) Reactive carbonyl species mediate ABA signaling in guard cells. Plant Cell Physiol 57:2552–2563

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nagar P, Sharma A, Batth R, Aggarwa S, Kumari S, Mustafz A (2018) GLYI and D-LDH play key role in methylglyoxal detoxifcation and abiotic stress tolerance. Sci Rep 8:5451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin SH, Li XQ, Wang GG, Zhu XT (2015) Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems. AoB Plants 7:plv009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaur C, Singla-Pareek SL, Sopory SK (2014) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. Crit Rev Plant Sci 33:429–456

    Article  CAS  Google Scholar 

  • Kaur C, Kushwaha HR, Mustafiz A, Pareek A, Sopory SK, Singla-Pareek SL (2015) Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule. Front Plant Sci 6:682

    PubMed  PubMed Central  Google Scholar 

  • Li ZG (2016) Methylglyoxal and glyoxalase system in plants: old players, new concepts. Bot Rev 82:183–203

    Article  Google Scholar 

  • Li ZG, Duan XQ, Xia YM, Wang Y, Zhou ZH, Min X (2017) Methylglyoxal alleviates cadmium toxicity in wheat (Triticum aestivum L). Plant Cell Rep 36:367–370

    Article  PubMed  CAS  Google Scholar 

  • Li ZG, Nie Q, Yang CL, Wang Y, Zhou ZH (2018) Signaling molecule methylglyoxal ameliorates cadmium injury in wheat (Triticum aestivum L) by a coordinated induction of glutathione pool and glyoxalase system. Ecotoxicol Environ Saf 149:101–107

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Xu Y, Bai LK, Zhang SY, Wang Y (2019) Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems. Protoplasma 256:471–490

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Xiang RH, Wang JQ (2021) Hydrogen sulfide–phytohormone interaction in plants ender physiological and stress conditions. J Plant Growth Regul (in press)

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620

    Article  CAS  PubMed  Google Scholar 

  • Maeta K, Mori K, Takatsume Y, Izawa S, Inoue Y (2005) Diagnosis of cell death induced by methylglyoxal, ametabolite derived from glycolysis, in Saccharomyces cerevisiae. FEMS Microbiol Lett 243:87–92

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Yoshida N, Fujita M (2014) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44

    Article  CAS  Google Scholar 

  • Mostofa MG, Ghosh A, Li ZG, Siddiqui MN, Fujita M, Tran LSP (2018) Methylglyoxal-a signaling molecule in plant abiotic stress response. Free Radic Biol Med 212:96–109

    Article  CAS  Google Scholar 

  • Mustafiz A, Singh AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) Genome-wide analysis of rice and Arabidopsis identifies two glyoxalase genes that are highly expressed in abiotic stresses. Funct Integr Genom 11:293–305

    Article  CAS  Google Scholar 

  • Nadarajah KK (2020) ROS homeostasis in abiotic stress tolerance in plants. Int J Mol Sci 21:5208

    Article  CAS  PubMed Central  Google Scholar 

  • 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 112:44–54

    Article  CAS  Google Scholar 

  • 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 254:445–460

    Article  CAS  PubMed  Google Scholar 

  • Nareshkumar A, Subbarao S, Vennapusa AR, Ashwin V, Banarjee R, Kulkarni MJ, Ramu VS, Udayakumar M (2020) Enzymatic and non-enzymatic detoxifcation of reactive carbonyl compounds improves the oxidative stress tolerance in cucumber, tobacco and rice seedlings. J Plant Growth Regul (in press)

  • Nguyen TM, Bressac C, Chevrier C (2013) Heat stress affects male reproduction in a parasitoid wasp. J Insect Physiol 59:248–254

    Article  CAS  PubMed  Google Scholar 

  • Oberschall A, Deak M, Torok K, Sass L, Vass I, Kovacs I, Feher A, Dudits D, Horvath GV (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stress. Plant J 24:437–446

    Article  CAS  PubMed  Google Scholar 

  • Shumilina J, Kusnetsova A, Tsarev A, Janse van Rensburg HC, Medvedev S, Demidchik V, Van den Ende WV, Frolov A (2019) Glycation of plant proteins: regulatory roles and interplay with sugar signalling? Int J Mol Sci 20:2366

    Article  CAS  PubMed Central  Google Scholar 

  • Simpson PJ, Tantitadapitak C, Reed AM, Mather OC, Bunce CM, White SA, Ride JP (2009) Characterization of two novel aldo-keto reductases from Arabidopsis: expression patterns, broad substrate specificity, and an open active-site structure suggest a role in toxicant metabolism following stress. J Mol Biol 392:465–480

    Article  CAS  PubMed  Google Scholar 

  • Sudnitsyna MV, Gusev NB (2017) Methylglyoxal and small heat shock proteins. Biochem Mosc 82:751–759

    Article  CAS  Google Scholar 

  • Takagi D, Inoue H, Odawara M, Shimakawa G, Miyake C (2014) The Calvin cycle inevitably produces sugar derived reactive carbonyl methylglyoxal during photosynthesis: a potential cause of plant diabetes. Plant Cell Physiol 55:333–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tardieu F, Tuberosa R (2010) Dissection and modelling of abiotic stress tolerance in plants. Curr Opin Plant Biol 13:206–212

    Article  PubMed  Google Scholar 

  • Turoczy Z, Kis P, Torok K, Cserhati M, Lendvai A, Dudits D, Horvath GV (2011) Overproduction of a rice aldo–keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification. Plant Mol Biol 75:399–412

    Article  CAS  PubMed  Google Scholar 

  • Vadakkancherry MM, Pushpanathan A, Peter CS, Selvarajan D, Jayanarayanan AN, Markandan M, Ramalingam S, Giriyapura SS, Govind H, Bakshi R, Chinnaswamy A (2019) Comparative analysis of glyoxalase pathway genes in Erianthus arundinaceus and commercial sugarcane hybrid under salinity and drought conditions. BMC Genom 19:986

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wang Y, Ye XY, Qiu XM, Li ZG (2019) Methylglyoxal triggers the heat tolerance in maize seedlings by driving AsA-GSH cycle and reactive oxygen species-/methylglyoxal-scavenging system. Plant Physiol Biochem 138:91–99

    Article  CAS  PubMed  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in Plants. J Biol Chem 286:6999–7009

    Article  CAS  PubMed  Google Scholar 

  • Yan G, Lv X, Gao G, Li F, Li J, Qiao J, Xu K, Chen B, Wang L, Xiao X, Wu X (2016) Identification and characterization of a glyoxalase I gene in a rapeseed cultivar with seed thermotolerance. Front Plant Sci 7:15

    Google Scholar 

  • Yan G, Xiao X, Wang N, Zhang F, Gao G, Xu K, Chen B, Qiao J, Wu X (2018) Genome-wide analysis and expression profiles of glyoxalase gene families in Chinese cabbage (Brassica rapa L.). PLoS ONE 13:e0191159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ye XY, Qiu XM, Sun YY, Li ZG (2020) Interplay between hydrogen sulfide and methylglyoxal initiates thermotolerance in maize seedlings by modulating reactive oxidative species and osmolyte metabolism. Protoplasma 257:1415–1432

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work is funded by National Natural Science Foundation of China (31760069). I am thankful to the scientists whose excellent work has been cited in this paper, but I regret that the other excellent work cannot be cited due to space limitation.

Author information

Authors and Affiliations

  1. School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China

    Zhong-Guang Li

  2. Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China

    Zhong-Guang Li

  3. Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Normal University, Kunming, 650092, Yunnan, People’s Republic of China

    Zhong-Guang Li

Authors
  1. Zhong-Guang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhong-Guang Li.

Ethics declarations

Conflict of interest

The author declares that there is no conflict of interest.

Additional information

Communicated by S. Esposito.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, ZG. Role of methylglyoxal and its detoxification system in plant thermotolerance. Acta Physiol Plant 44, 69 (2022). https://doi.org/10.1007/s11738-022-03407-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-022-03407-5

Keywords

Search

Navigation