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Hydrogen peroxide is involved in methane-induced tomato lateral root formation

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Abstract

Key message

Pharmacological and molecular evidence reveals a novel role of methane (CH4) gas in root organogenesis, the induction of lateral root (LR) formation, and this response might require hydrogen peroxide (H2O2) synthesis.

Abstract

Although plants can produce CH4 and release this to atmosphere, the beneficial role(s) of CH4 are not fully elucidated. In this study, the fumigation with CH4 not only increased NADPH oxidase activity and H2O2 production, but also induced tomato lateral root primordial formation and thereafter LR development. However, exogenously applied argon and nitrogen failed to influence LR formation. Above responses triggered by CH4 were sensitive to the removal of endogenous H2O2 with dimethylthiourea (DMTU; a membrane-permeable scavenger of H2O2), suggesting the hypothesis that CH4’s effect on LR formation could be mediated by endogenous H2O2. Diphenylene iodonium (DPI) inhibition of the H2O2 generating enzyme NADPH oxidase attenuated H2O2 synthesis and impaired LR formation in response to CH4, confirming the requirement of NADPH oxidase-dependent H2O2. Meanwhile, the alterations of endogenous H2O2 concentrations failed to influence CH4 production in tomato seedlings. Molecular evidence revealed that CH4-induced SlCDKA1, SlCYCA2;1, and SlCYCA3;1 transcripts, and -decreased SlKRP2 mRNA were impaired by DMTU or DPI. Contrasting changes in LR formation-related miR390a and miR160 transcripts and their target genes, including SlARF4 and SlARF16, were observed. Together, our pharmacological and molecular evidence suggested the requirement of H2O2 synthesis in CH4-triggered tomato LR formation, partially via the regulation of cell cycle regulatory genes, miRNA-, and tasiRNA-modulated gene expression.

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Abbreviations

Ar:

Argon

ARFs:

Auxin response factors

CH4 :

Methane

DMTU:

Dimethylthiourea

DPI:

Diphenylene iodonium

H2DCF-DA:

2′,7′-Dichlorofluorescein diacetate

H2O2 :

Hydrogen peroxide

LR:

Lateral root

LRP:

Lateral root primordia

LSCM:

Laser scanning confocal microscopy

MiRNAs:

MicroRNAs

N2 :

Nitrogen

PR:

Primary root

qPCR:

Quantitative real-time RT-PCR

ROS:

Reactive oxygen species

TasiRNAs:

Transacting short-interfering RNAs

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Acknowledgements

This work was supported by the Natural Science Foundation of Jiangsu Province (Grant no.: BK20181317) and the National Natural Science Foundation of China (31772292).

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Authors and Affiliations

  1. College of Life Sciences, Laboratory Center of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Yingying Zhao, Yihua Zhang, Feijie Liu & Wenbiao Shen

  2. Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China

    Ren Wang

  3. College of Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Liqin Huang

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  1. Yingying Zhao
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Zhao, Y., Zhang, Y., Liu, F. et al. Hydrogen peroxide is involved in methane-induced tomato lateral root formation. Plant Cell Rep 38, 377–389 (2019). https://doi.org/10.1007/s00299-019-02372-7

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