Transcriptomic analysis reveals the regulatory mechanisms of messenger RNA (mRNA) and long non-coding RNA (lncRNA) in response to waterlogging stress in rye (Secale cereale L.).


Journal

BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807

Informations de publication

Date de publication:
12 Jun 2024
Historique:
received: 09 03 2024
accepted: 03 06 2024
medline: 12 6 2024
pubmed: 12 6 2024
entrez: 11 6 2024
Statut: epublish

Résumé

Waterlogging stress (WS) negatively impacts crop growth and productivity, making it important to understand crop resistance processes and discover useful WS resistance genes. In this study, rye cultivars and wild rye species were subjected to 12-day WS treatment, and the cultivar Secale cereale L. Imperil showed higher tolerance. Whole transcriptome sequencing was performed on this cultivar to identify differentially expressed (DE) messenger RNAs (DE-mRNAs) and long non-coding RNAs (DE-lncRNAs) involved in WS response. Among the 6 species, Secale cereale L. Imperil showed higher tolerance than wild rye species against WS. The cultivar effectively mitigated oxidative stress, and regulated hydrogen peroxide and superoxide anion. A total of 728 DE-mRNAs and 60 DE-lncRNAs were discovered. Among these, 318 DE-mRNAs and 32 DE-lncRNAs were upregulated, and 410 DE-mRNAs and 28 DE-lncRNAs were downregulated. GO enrichment analysis discovered metabolic processes, cellular processes, and single-organism processes as enriched biological processes (BP). For cellular components (CC), the enriched terms were membrane, membrane part, cell, and cell part. Enriched molecular functions (MF) terms were catalytic activity, binding, and transporter activity. LncRNA and mRNA regulatory processes were mainly related to MAPK signaling pathway-plant, plant hormone signal transduction, phenylpropanoid biosynthesis, anthocyanin biosynthesis, glutathione metabolism, ubiquitin-mediated proteolysis, ABC transporter, Cytochrome b6/f complex, secondary metabolite biosynthesis, and carotenoid biosynthesis pathways. The signalling of ethylene-related pathways was not mainly dependent on AP2/ERF and WRKY transcription factors (TF), but on other factors. Photosynthetic activity was active, and carotenoid levels increased in rye under WS. Sphingolipids, the cytochrome b6/f complex, and glutamate are involved in rye WS response. Sucrose transportation was not significantly inhibited, and sucrose breakdown occurs in rye under WS. This study investigated the expression levels and regulatory functions of mRNAs and lncRNAs in 12-day waterlogged rye seedlings. The findings shed light on the genes that play a significant role in rye ability to withstand WS. The findings from this study will serve as a foundation for further investigations into the mRNA and lncRNA WS responses in rye.

Sections du résumé

BACKGROUND BACKGROUND
Waterlogging stress (WS) negatively impacts crop growth and productivity, making it important to understand crop resistance processes and discover useful WS resistance genes. In this study, rye cultivars and wild rye species were subjected to 12-day WS treatment, and the cultivar Secale cereale L. Imperil showed higher tolerance. Whole transcriptome sequencing was performed on this cultivar to identify differentially expressed (DE) messenger RNAs (DE-mRNAs) and long non-coding RNAs (DE-lncRNAs) involved in WS response.
RESULTS RESULTS
Among the 6 species, Secale cereale L. Imperil showed higher tolerance than wild rye species against WS. The cultivar effectively mitigated oxidative stress, and regulated hydrogen peroxide and superoxide anion. A total of 728 DE-mRNAs and 60 DE-lncRNAs were discovered. Among these, 318 DE-mRNAs and 32 DE-lncRNAs were upregulated, and 410 DE-mRNAs and 28 DE-lncRNAs were downregulated. GO enrichment analysis discovered metabolic processes, cellular processes, and single-organism processes as enriched biological processes (BP). For cellular components (CC), the enriched terms were membrane, membrane part, cell, and cell part. Enriched molecular functions (MF) terms were catalytic activity, binding, and transporter activity. LncRNA and mRNA regulatory processes were mainly related to MAPK signaling pathway-plant, plant hormone signal transduction, phenylpropanoid biosynthesis, anthocyanin biosynthesis, glutathione metabolism, ubiquitin-mediated proteolysis, ABC transporter, Cytochrome b6/f complex, secondary metabolite biosynthesis, and carotenoid biosynthesis pathways. The signalling of ethylene-related pathways was not mainly dependent on AP2/ERF and WRKY transcription factors (TF), but on other factors. Photosynthetic activity was active, and carotenoid levels increased in rye under WS. Sphingolipids, the cytochrome b6/f complex, and glutamate are involved in rye WS response. Sucrose transportation was not significantly inhibited, and sucrose breakdown occurs in rye under WS.
CONCLUSIONS CONCLUSIONS
This study investigated the expression levels and regulatory functions of mRNAs and lncRNAs in 12-day waterlogged rye seedlings. The findings shed light on the genes that play a significant role in rye ability to withstand WS. The findings from this study will serve as a foundation for further investigations into the mRNA and lncRNA WS responses in rye.

Identifiants

pubmed: 38862913
doi: 10.1186/s12870-024-05234-x
pii: 10.1186/s12870-024-05234-x
doi:

Substances chimiques

RNA, Long Noncoding 0
RNA, Messenger 0
RNA, Plant 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

534

Informations de copyright

© 2024. The Author(s).

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Auteurs

Daniel Bimpong (D)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Lili Zhao (L)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Mingyang Ran (M)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Xize Zhao (X)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Cuicui Wu (C)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Ziqun Li (Z)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Xue Wang (X)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Ling Cheng (L)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Zhengwu Fang (Z)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Zanmin Hu (Z)

State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.

Chengming Fan (C)

State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.

Bernard Gyebi-Nimako (B)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Yirou Luo (Y)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China.

Shuping Wang (S)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China. wangshuping2003@126.com.

Yingxin Zhang (Y)

College of Agriculture, Yangtze University, Jingzhou, 434000, Hubei, China. zhangyingxin1985@126.com.

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