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Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress

BACKGROUND: Recently, pine wood nematode (PWN, Bursaphelenchus xylophilus) has been found in the extreme cold area of northeast China. The third-stage dispersal juvenile (DJ3) of PWN, which is a long-lived stress-resistant stage, plays an important role in the process of PWN spreading to low-tempera...

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Autores principales: Chen, Qiaoli, Zhang, Ruizhi, Li, Danlei, Wang, Feng, Jiang, Shengwei, Wang, Jianan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8268229/
https://www.ncbi.nlm.nih.gov/pubmed/34243706
http://dx.doi.org/10.1186/s12864-021-07839-0
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author Chen, Qiaoli
Zhang, Ruizhi
Li, Danlei
Wang, Feng
Jiang, Shengwei
Wang, Jianan
author_facet Chen, Qiaoli
Zhang, Ruizhi
Li, Danlei
Wang, Feng
Jiang, Shengwei
Wang, Jianan
author_sort Chen, Qiaoli
collection PubMed
description BACKGROUND: Recently, pine wood nematode (PWN, Bursaphelenchus xylophilus) has been found in the extreme cold area of northeast China. The third-stage dispersal juvenile (DJ3) of PWN, which is a long-lived stress-resistant stage, plays an important role in the process of PWN spreading to low-temperature areas, as this stage can survive under unfavorable conditions. RESULTS: Weighted correlation network analysis (WGCNA) was used to analyze the expression patterns of 15,889 genes included in 21 RNA-Seq results of PWN at DJ3 and the other 6 different stages, and a total of 12 coexpression modules were obtained. Among them, the magenta module has the highest correlation with DJ3, which included a total of 652 genes. KEGG enrichment analysis showed that most of the genes in the magenta module were involved in metabolic processes, which were related to autophagy and longevity regulation. These pathways included starch and sucrose metabolism, which contains trehalose metabolism. To explore the function of trehalose in DJ3 formation and survival under − 20 °C, a trehalose-6-phosphate synthase encoding gene (Bx-tps), a trehalose-6-phosphate phosphatase encoding gene (Bx-tpp) and 7 trehalase encoding genes (Bx-tres) were identified and investigated. The expression of these 9 genes was related to the formation of DJ3. A treatment under − 20 °C induced the accumulation of trehalose. The survival rate of DJ3 at -20 °C reduced after silencing of any of these trehalose metabolism genes. Further analysis suggested that two trehalose synthesis genes were highly correlated with DJ3 and might be involved in autophagy by regulating with energy conversion related genes. CONCLUSIONS: The above results indicated that trehalose metabolism promotes DJ3 formation and helps DJ3 survive at -20 °C. Although trehalose accumulation is favorable for DJ3 to cope with low-temperature stress, multiple trehalose metabolism genes need to work together. There may be a multi-path regulated physiological process involving trehalose synthesis genes under low-temperature stress resistance. This physiological process may regulate the formation and maintenance of DJ3 through autophagy and energy conversion. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07839-0.
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spelling pubmed-82682292021-07-09 Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress Chen, Qiaoli Zhang, Ruizhi Li, Danlei Wang, Feng Jiang, Shengwei Wang, Jianan BMC Genomics Research Article BACKGROUND: Recently, pine wood nematode (PWN, Bursaphelenchus xylophilus) has been found in the extreme cold area of northeast China. The third-stage dispersal juvenile (DJ3) of PWN, which is a long-lived stress-resistant stage, plays an important role in the process of PWN spreading to low-temperature areas, as this stage can survive under unfavorable conditions. RESULTS: Weighted correlation network analysis (WGCNA) was used to analyze the expression patterns of 15,889 genes included in 21 RNA-Seq results of PWN at DJ3 and the other 6 different stages, and a total of 12 coexpression modules were obtained. Among them, the magenta module has the highest correlation with DJ3, which included a total of 652 genes. KEGG enrichment analysis showed that most of the genes in the magenta module were involved in metabolic processes, which were related to autophagy and longevity regulation. These pathways included starch and sucrose metabolism, which contains trehalose metabolism. To explore the function of trehalose in DJ3 formation and survival under − 20 °C, a trehalose-6-phosphate synthase encoding gene (Bx-tps), a trehalose-6-phosphate phosphatase encoding gene (Bx-tpp) and 7 trehalase encoding genes (Bx-tres) were identified and investigated. The expression of these 9 genes was related to the formation of DJ3. A treatment under − 20 °C induced the accumulation of trehalose. The survival rate of DJ3 at -20 °C reduced after silencing of any of these trehalose metabolism genes. Further analysis suggested that two trehalose synthesis genes were highly correlated with DJ3 and might be involved in autophagy by regulating with energy conversion related genes. CONCLUSIONS: The above results indicated that trehalose metabolism promotes DJ3 formation and helps DJ3 survive at -20 °C. Although trehalose accumulation is favorable for DJ3 to cope with low-temperature stress, multiple trehalose metabolism genes need to work together. There may be a multi-path regulated physiological process involving trehalose synthesis genes under low-temperature stress resistance. This physiological process may regulate the formation and maintenance of DJ3 through autophagy and energy conversion. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07839-0. BioMed Central 2021-07-09 /pmc/articles/PMC8268229/ /pubmed/34243706 http://dx.doi.org/10.1186/s12864-021-07839-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Chen, Qiaoli
Zhang, Ruizhi
Li, Danlei
Wang, Feng
Jiang, Shengwei
Wang, Jianan
Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title_full Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title_fullStr Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title_full_unstemmed Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title_short Trehalose in pine wood nematode participates in DJ3 formation and confers resistance to low-temperature stress
title_sort trehalose in pine wood nematode participates in dj3 formation and confers resistance to low-temperature stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8268229/
https://www.ncbi.nlm.nih.gov/pubmed/34243706
http://dx.doi.org/10.1186/s12864-021-07839-0
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