Crosstalk between melatonin and nitric oxide restrains Cadmium-induced oxidative stress and enhances vinblastine biosynthesis in Catharanthus roseus (L) G Don.

Nabaei, Masoomeh; Amooaghaie, Rayhaneh; Ghorbanpour, Mansour; Ahadi, Alimohammad

doi:10.1007/s00299-024-03229-4

Crosstalk between melatonin and nitric oxide restrains Cadmium-induced oxidative stress and enhances vinblastine biosynthesis in Catharanthus roseus (L) G Don.

Original Article
Published: 13 May 2024

Volume 43, article number 139, (2024)
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Masoomeh Nabaei¹,
Rayhaneh Amooaghaie ORCID: orcid.org/0000-0002-8575-5407^1,2,
Mansour Ghorbanpour³ &
…
Alimohammad Ahadi⁴

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Abstract

Key message

Nitric oxide functions downstream of the melatonin in adjusting Cd-induced osmotic and oxidative stresses, upregulating the transcription of D4H and DAT genes, and increasing total alkaloid and vincristine contents.

Abstract

A few studies have investigated the relationship between melatonin (MT) and nitric oxide (NO) in regulating defensive responses. However, it is still unclear how MT and NO interact to regulate the biosynthesis of alkaloids and vincristine in leaves of Catharanthus roseus (L.) G. Don under Cd stress. Therefore, this context was explored in the present study. Results showed that Cd toxicity (200 µM) induced oxidative stress, decreased biomass, Chl a, and Chl b content, and increased the content of total alkaloid and vinblastine in the leaves. Application of both MT (100 µM) and sodium nitroprusside (200 µM SNP, as NO donor) enhanced endogenous NO content and accordingly increased metal tolerance index, the content of total alkaloid and vinblastine. It also upregulated the transcription of two respective genes (D4H and DAT) under non-stress and Cd stress conditions. Moreover, the MT and SNP treatments reduced the content of H₂O₂ and malondialdehyde, increased the activities of superoxide dismutase and ascorbate peroxidase, enhanced proline accumulation, and improved relative water content in leaves of Cd-exposed plants. The scavenging NO by 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l-3-oxide (cPTIO) averted the effects of MT on the content of total alkaloid and vinblastine and antioxidative responses. Still, the effects conferred by NO on attributes mentioned above were not significantly impaired by p–chlorophenylalanine (p-CPA as an inhibitor of MT biosynthesis). These findings and multivariate analyses indicate that MT motivated terpenoid indole alkaloid biosynthesis and mitigated Cd-induced oxidative stress in the leaves of periwinkle in a NO-dependent manner.

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Data availability

The data that support the findings of this study are available from the first author upon reasonable request.

Abbreviations

APX:: Ascorbate peroxidase
CAT:: Catalase
Cd:: Cadmium
Chl.:: Chlorophyll
cPTIO:: 4-Carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide
D-4H:: Desacetoxylvindoline-4 hydroxylase
DAT:: Deacetylvindoline acetyl CoA acetyltransferase
DW:: Dry weight
FW:: Fresh weight
HM:: Heavy metals
MAPKs:: Mitogen-activated protein kinases
MDA:: Malondialdehyde
MT:: Melatonin
MTI:: Metal tolerance index
NBT:: Nitroblue tetrazolium
NO:: Nitric oxide
NOMET:: N-Nitrosomelatonin
NOS:: Nitric oxide synthase
NR:: Nitrate reductase
nSiO₂ :: Silicon dioxide nanoparticles
p-CPA:: P–chlorophenylalanine
POD:: Peroxidase
PRX1:: Peroxidase 1
PTMs:: Post-translational modifications
ROS:: Reactive oxygen species
RWC:: Relative water content
SNP:: Sodium nitroprusside
SOD:: Superoxide dismutase
STR:: Strictosidine synthase
TBA:: Thiobarbituric acid
TIA:: Terpenoid indole alkaloid
TW:: Turgor weight

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The authors would like to thank the Plant Science Department of Shahrekord University, Iran, for the financial support of this research.

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Plant Science Department, Faculty of Science, Shahrekord University, Shahrekord, Iran
Masoomeh Nabaei & Rayhaneh Amooaghaie
Biotechnology Research Institute, Shahrekord University, Shahrekord, Iran
Rayhaneh Amooaghaie
Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, 38156-8-8349, Iran
Mansour Ghorbanpour
Genetic Department, Science Faculty, Shahrekord University, Shahrekord, Iran
Alimohammad Ahadi

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Masoomeh Nabaei
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RA conceived and designed research. MN conducted experiments. AA and MG advised and contributed to RT-PCR and statistical analysis, respectively. RA and MN analyzed data and wrote the manuscript and M.Gh. edited it. All authors read and approved the manuscript.

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Nabaei, M., Amooaghaie, R., Ghorbanpour, M. et al. Crosstalk between melatonin and nitric oxide restrains Cadmium-induced oxidative stress and enhances vinblastine biosynthesis in Catharanthus roseus (L) G Don.. Plant Cell Rep 43, 139 (2024). https://doi.org/10.1007/s00299-024-03229-4

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Received: 29 February 2024
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Published: 13 May 2024
DOI: https://doi.org/10.1007/s00299-024-03229-4

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Crosstalk between melatonin and nitric oxide restrains Cadmium-induced oxidative stress and enhances vinblastine biosynthesis in Catharanthus roseus (L) G Don.