Alleviation of Oxidative Stress Induced by 24-Epibrassinolide in Soybean Plants Exposed to Different Manganese Supplies: UpRegulation of Antioxidant Enzymes and Maintenance of Photosynthetic Pigments

Abstract

Adverse effects promoted by inadequate manganese (Mn) supply (deficiency or toxicity) causes inefficiency of the antioxidant system and degradation of chlorophylls. However, 24-epibrassinolide (EBR) is a natural steroid that exhibits beneficial effects on antioxidant metabolism, chlorophyll levels and stress indicators. Therefore, this research aims to evaluate whether EBR application via spray can alleviate oxidative stress in soybean plants exposed to different Mn concentrations and to determine possible contributions of the antioxidant enzymes and photosynthetic pigments. Experiment followed a completely randomized factorial design with two concentrations of 24-epibrassinolide (0 and 100 nM EBR, described as − EBR and + EBR, respectively) and three Mn doses (0.25, 25 and 2500 µM Mn, described as low, control and high supply of Mn, respectively). Plants treated with low and high concentrations of Mn + EBR exhibit significant increases in all enzymes evaluated (superoxide dismutase, catalase, ascorbate peroxidase and peroxidase). To superoxide dismutase (SOD), EBR spray promoted increments of 77%, 38% and 76% under low, control and high Mn supplementation, respectively, compared to same treatment in absence of EBR. Clearly intense activity is linked to SOD contributed by dismutation of superoxide into hydrogen peroxide, being subsequently decomposed by other enzymes (catalase, ascorbate peroxidase and peroxidase). Concomitantly, plants with Mn deficiency and toxicity sprayed with 100 nM EBR presented maintenance of chlorophylls and carotenoids due to reduction of superoxide and hydrogen peroxide and consequently reduced chloroplast membrane damages as indicated by malondialdehyde levels and electrolyte leakage.

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Data Availability

Data are available upon request to the corresponding author.

Abbreviations

APX:

Ascorbate peroxidase

B:

Boron

BRs:

Brassinosteroids

Ca:

Calcium

Ca(NO3)2 :

Calcium nitrate

CAR:

Carotenoids

CAT:

Catalase

Cd:

Cadmium

CDF:

Cation diffusion facilitators

Chl a :

Chlorophyll a

Chl b :

Chlorophyll b

C i :

Intercellular CO2 concentration

CO2 :

Carbon dioxide

E :

Transpiration rate

EBR:

24-Epibrassinolide

EL:

Electrolyte leakage

ETR:

Electron transport rate

ETR/PN :

Ratio between the apparent electron transport rate and net photosynthetic rate

EXC:

Relative energy excess at the PSII level

F 0 :

Minimal fluorescence yield of the dark-adapted state

Fe:

Iron

F m :

Maximal fluorescence yield of the dark-adapted state

F v :

Variable fluorescence

Fv/Fm :

Maximal quantum yield of PSII photochemistry

gs :

Stomatal conductance

H2O2 :

Hydrogen peroxide

K:

Potassium

LDM:

Leaf dry matter

MDA:

Malondialdehyde

Mg:

Magnesium

Mn:

Manganese

Mo:

Molybdenum

NADP + :

Nicotinamide adenine dinucleotide phosphate

NPQ:

Nonphotochemical quenching

\({\text{O}}_{2}^{ - }\) :

Superoxide

O2 :

Oxygen

P:

Phosphorus

P N :

Net photosynthetic rate

PN/Ci :

Instantaneous carboxylation efficiency

POX:

Peroxidase

PSII:

Photosystem II

q P :

Photochemical quenching

RDM:

Root dry matter

ROS:

Reactive oxygen species

SDM:

Stem dry matter

SH:

Sulfhydryl

SOD:

Superoxide dismutase

TDM:

Total dry matter

Total Chl:

Total chlorophyll

WUE:

Water-use efficiency

Zn:

Zinc

Φ PSII :

Effective quantum yield of PSII photochemistry

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Acknowledgements

This research had financial supports from Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil) and Universidade Federal Rural da Amazônia (UFRA/Brazil) to AKSL. While WSR and YCP were supported by scholarships from Programa de Educação Tutorial (PET/Brazil).

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AKSL was advisor of this project, planning all phases of this research. WSR, YCP and ALMS conducted the experiment in the greenhouse and performed physiological, biochemical and morphological determinations. BLB carried out nutritional determinations and helped in drafting the manuscript and in interpreting the results.

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Correspondence to Allan Klynger da Silva Lobato.

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Rodrigues, W.S., Pereira, Y.C., de Souza, A.L.M. et al. Alleviation of Oxidative Stress Induced by 24-Epibrassinolide in Soybean Plants Exposed to Different Manganese Supplies: UpRegulation of Antioxidant Enzymes and Maintenance of Photosynthetic Pigments. J Plant Growth Regul 39, 1425–1440 (2020). https://doi.org/10.1007/s00344-020-10091-7

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Keywords

  • Antioxidant system
  • Brassinosteroids
  • Chlorophylls
  • Glycine max
  • Hydrogen peroxide
  • Stress indicators
  • Superoxide