Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings

Abstract Background Both hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) are separately regarded as a highly reactive molecule involved in root morphogenesis. In this report, corresponding causal link governing lateral root formation was investigated. Methods By using pharmacological, anatomic,...

Full description

Bibliographic Details
Main Authors: Yudong Mei, Haotian Chen, Wenbiao Shen, Wei Shen, Liqin Huang
Format: Article
Language:English
Published: BMC 2017-10-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-017-1110-7
_version_ 1811268466719588352
author Yudong Mei
Haotian Chen
Wenbiao Shen
Wei Shen
Liqin Huang
author_facet Yudong Mei
Haotian Chen
Wenbiao Shen
Wei Shen
Liqin Huang
author_sort Yudong Mei
collection DOAJ
description Abstract Background Both hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) are separately regarded as a highly reactive molecule involved in root morphogenesis. In this report, corresponding causal link governing lateral root formation was investigated. Methods By using pharmacological, anatomic, and molecular approaches, evidence presented here revealed the molecular mechanism underlying tomato lateral root development triggered by H2S. Results A H2S donor sodium hydrosulfide (NaHS) triggered the accumulation of H2O2, the up-regulation of RBOH1 transcript, and thereafter tomato lateral root formation. Above responses were sensitive to the H2O2 scavenger (dimethylthiourea; DMTU) and the inhibitor of NADPH oxidase (diphenylene idonium; DPI), showing that the accumulations of H2O2 and increased RBOH1 transcript were respectively prevented. Lateral root primordial and lateral root formation were also impaired. Further molecular evidence revealed that H2S-modulated gene expression of cell cycle regulatory genes, including up-regulation of SlCYCA2;1, SlCYCA3;1, and SlCDKA1, and the down-regulation of SlKRP2, were prevented by the co-treatment with DMTU or DPI. Above mentioned inducing phenotypes were consistent with the changes of lateral root formation-related microRNA transcripts: up-regulation of miR390a and miR160, and with the opposite tendencies of their target genes (encoding auxin response factors). Contrasting tendencies were observed when DMTU or DPI was added together. The occurrence of H2S-mediated S-sulfhydration during above responses was preliminarily discovered. Conclusions Overall, these results suggested an important role of RBOH1-mediated H2O2 in H2S-elicited tomato lateral root development, and corresponding H2S-target proteins regulated at transcriptional and post-translational levels.
first_indexed 2024-04-12T21:23:24Z
format Article
id doaj.art-3118b18579c746c39e2b074a597173ea
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-04-12T21:23:24Z
publishDate 2017-10-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-3118b18579c746c39e2b074a597173ea2022-12-22T03:16:14ZengBMCBMC Plant Biology1471-22292017-10-0117111210.1186/s12870-017-1110-7Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlingsYudong Mei0Haotian Chen1Wenbiao Shen2Wei Shen3Liqin Huang4College of Life Sciences, Laboratory Center of Life Sciences, Nanjing Agricultural UniversityCollege of Sciences, Nanjing Agricultural UniversityCollege of Life Sciences, Laboratory Center of Life Sciences, Nanjing Agricultural UniversityCollege of Sciences, Nanjing Agricultural UniversityCollege of Sciences, Nanjing Agricultural UniversityAbstract Background Both hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) are separately regarded as a highly reactive molecule involved in root morphogenesis. In this report, corresponding causal link governing lateral root formation was investigated. Methods By using pharmacological, anatomic, and molecular approaches, evidence presented here revealed the molecular mechanism underlying tomato lateral root development triggered by H2S. Results A H2S donor sodium hydrosulfide (NaHS) triggered the accumulation of H2O2, the up-regulation of RBOH1 transcript, and thereafter tomato lateral root formation. Above responses were sensitive to the H2O2 scavenger (dimethylthiourea; DMTU) and the inhibitor of NADPH oxidase (diphenylene idonium; DPI), showing that the accumulations of H2O2 and increased RBOH1 transcript were respectively prevented. Lateral root primordial and lateral root formation were also impaired. Further molecular evidence revealed that H2S-modulated gene expression of cell cycle regulatory genes, including up-regulation of SlCYCA2;1, SlCYCA3;1, and SlCDKA1, and the down-regulation of SlKRP2, were prevented by the co-treatment with DMTU or DPI. Above mentioned inducing phenotypes were consistent with the changes of lateral root formation-related microRNA transcripts: up-regulation of miR390a and miR160, and with the opposite tendencies of their target genes (encoding auxin response factors). Contrasting tendencies were observed when DMTU or DPI was added together. The occurrence of H2S-mediated S-sulfhydration during above responses was preliminarily discovered. Conclusions Overall, these results suggested an important role of RBOH1-mediated H2O2 in H2S-elicited tomato lateral root development, and corresponding H2S-target proteins regulated at transcriptional and post-translational levels.http://link.springer.com/article/10.1186/s12870-017-1110-7Hydrogen sulfide (H2S)Hydrogen peroxide (H2O2)Solanum lycopersicumLateral root formationmiRNAS-sulfhydration
spellingShingle Yudong Mei
Haotian Chen
Wenbiao Shen
Wei Shen
Liqin Huang
Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
BMC Plant Biology
Hydrogen sulfide (H2S)
Hydrogen peroxide (H2O2)
Solanum lycopersicum
Lateral root formation
miRNA
S-sulfhydration
title Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
title_full Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
title_fullStr Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
title_full_unstemmed Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
title_short Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings
title_sort hydrogen peroxide is involved in hydrogen sulfide induced lateral root formation in tomato seedlings
topic Hydrogen sulfide (H2S)
Hydrogen peroxide (H2O2)
Solanum lycopersicum
Lateral root formation
miRNA
S-sulfhydration
url http://link.springer.com/article/10.1186/s12870-017-1110-7
work_keys_str_mv AT yudongmei hydrogenperoxideisinvolvedinhydrogensulfideinducedlateralrootformationintomatoseedlings
AT haotianchen hydrogenperoxideisinvolvedinhydrogensulfideinducedlateralrootformationintomatoseedlings
AT wenbiaoshen hydrogenperoxideisinvolvedinhydrogensulfideinducedlateralrootformationintomatoseedlings
AT weishen hydrogenperoxideisinvolvedinhydrogensulfideinducedlateralrootformationintomatoseedlings
AT liqinhuang hydrogenperoxideisinvolvedinhydrogensulfideinducedlateralrootformationintomatoseedlings