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Brassinosteroids-Mediated Amelioration of Iron Deficiency in Soybean Plants: Beneficial Effects on the Nutritional Status, Photosynthetic Pigments and Chlorophyll Fluorescence

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Abstract

Iron (Fe) is essential for chlorophyll biosynthesis and functions in chloroplasts. Fe deficiency provokes negative effects on photochemical efficiency and electron transport. 24-Epibrassinolide (EBR) is a natural molecule with potential advantages, including a natural origin, biodegradability and high plant steroid bioactivity, improving metabolism and inducing tolerance during stress. Present study was aimed to investigate whether pre-treatment with EBR can trigger protective roles in soybean plants cultivated under the conditions of Fe deficiency and to evaluate the responses linked to the nutritional status, photosynthetic pigments and chlorophyll fluorescence. The study was carried out using a completely randomized design with four treatments (0 nM EBR + 250 µM Fe, 0 nM EBR + 2.5 µM Fe, 100 nM EBR + 250 µM Fe and 100 nM EBR + 2.5 µM Fe). Results revealed that the exogenous EBR minimized the damage caused by Fe deficiency. This steroid maximized the Fe content in the leaf, stem and root, as well as improved the nutrient content and metal homeostasis, as confirmed by the increased detection of Fe2+/Mg2+, Fe2+/Mn2+ and Fe2+/Cu2+ ratios in plants under Fe deficiency. Additionally, plants under Fe deficiency and sprayed with EBR had improvements on chloroplastic pigments, with significant increases in chlorophyll a (14%), chlorophyll b (23%), total chlorophyll (15%) and carotenoids (28%). Steroid also increased the photochemical efficiency, positively regulating electron transport and reducing the negative impacts associated with photoinhibition in photosystem II. Therefore, pre-treatment with EBR improved the nutrient contents and physiological performance of soybean plants under the conditions of Fe limitation.

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Data Availability

Data are available upon request to the corresponding author.

Abbreviations

APX:

Ascorbate peroxidase

BRs:

Brassinosteroids

CA:

Carbonic anhydrase

CAR:

Carotenoids

CAT:

Catalase

Chl a :

Chlorophyll a

Chl b :

Chlorophyll b

C i :

Intercellular CO2 concentration

CO2 :

Carbon dioxide

Cu:

Copper

E :

Transpiration rate

EBR:

24-Epibrassinolide

EDS:

Equatorial diameter of the stomata

EL:

Electrolyte leakage

ETAb:

Epidermis thickness from abaxial leaf side

ETAd:

Epidermis thickness from adaxial leaf side

ETR:

Electron transport rate

ETR/P N :

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

F v/F m :

Maximal quantum yield of PSII photochemistry

g s :

Stomatal conductance

H2O2 :

Hydrogen peroxide

K:

Potassium

LDM:

Leaf dry matter

MDA:

Malondialdehyde

Mg:

Magnesium

Mn:

Manganese

Mo:

Molybdenum

NPQ:

Nonphotochemical quenching

O2 :

Superoxide

P:

Phosphorus

PDS:

Polar diameter of the stomata

P N :

Net photosynthetic rate

P N/C i :

Instantaneous carboxylation efficiency

POX:

Peroxidase

PPT:

Palisade parenchyma thickness

PSII:

Photosystem II

q P :

Photochemical quenching

RCD:

Root cortex diameter

RDM:

Root dry matter

RMD:

Root metaxylem diameter

RDT:

Root endodermis thickness

RET:

Root epidermis thickness

ROS:

Reactive oxygen species

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SD:

Stomatal density

SDM:

Stem dry matter

SF:

Stomatal functionality

SI:

Stomatal index

SOD:

Superoxide dismutase

SPT:

Spongy parenchyma thickness

TDM:

Total dry matter

Total Chl:

Total Chlorophyll

VCD:

Vascular cylinder diameter

WUE:

Water-use efficiency

Zn:

Zinc

ΦPSII :

Effective quantum yield of PSII photochemistry

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Acknowledgements

This research was funded by Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), Programa de Pós-Graduação em Agronomia (PGAGRO/Brazil) and Universidade Federal Rural da Amazônia (UFRA/Brazil) to AKSL. Additionally, LRS was supported by a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/Brazil). Authors would like to extend their sincere appreciation to the Researches Supporting Project Number (RSP 2020/236) from King Saud University, Riyadh, Saudi Arabia.

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Contributions

AKSL was the advisor of this project, planning all phases of this research. LRS, LSP and YCP conducted the experiment in the greenhouse and performed physiological, biochemical and morphological determinations, while BRSS measured anatomical parameters and BLB performed nutritional determinations and helped in drafting the manuscript and in interpreting the results. AAA critically revised and edited the manuscript. All authors read and approved final version of manuscript.

Corresponding author

Correspondence to Allan Klynger da Silva Lobato.

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The authors declare that they have no competing interests.

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dos Santos, L.R., Paula, L.d.S., Pereira, Y.C. et al. Brassinosteroids-Mediated Amelioration of Iron Deficiency in Soybean Plants: Beneficial Effects on the Nutritional Status, Photosynthetic Pigments and Chlorophyll Fluorescence. J Plant Growth Regul 40, 1803–1823 (2021). https://doi.org/10.1007/s00344-020-10232-y

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