Cargando…

Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode

BACKGROUND: Ubiquitination is a major post-translational protein modification that regulates essentially all cellular and physiological pathways in eukaryotes. The ubiquitination process typically involves three distinct classes of enzymes, ubiquitin-activating enzyme (E1), ubiquitin-conjugating enz...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Chunyu, Song, Li, Choudhary, Mani Kant, Zhou, Bangjun, Sun, Guangchao, Broderick, Kyle, Giesler, Loren, Zeng, Lirong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6052599/
https://www.ncbi.nlm.nih.gov/pubmed/30021519
http://dx.doi.org/10.1186/s12870-018-1365-7
_version_ 1783340689098014720
author Zhang, Chunyu
Song, Li
Choudhary, Mani Kant
Zhou, Bangjun
Sun, Guangchao
Broderick, Kyle
Giesler, Loren
Zeng, Lirong
author_facet Zhang, Chunyu
Song, Li
Choudhary, Mani Kant
Zhou, Bangjun
Sun, Guangchao
Broderick, Kyle
Giesler, Loren
Zeng, Lirong
author_sort Zhang, Chunyu
collection PubMed
description BACKGROUND: Ubiquitination is a major post-translational protein modification that regulates essentially all cellular and physiological pathways in eukaryotes. The ubiquitination process typically involves three distinct classes of enzymes, ubiquitin-activating enzyme (E1), ubiquitin-conjugating enzyme (E2) and ubiquitin ligase (E3). To date, a comprehensive identification and analysis of core components comprising of the whole soybean (Glycine max) ubiquitin system (UBS) has not been reported. RESULTS: We performed a systematic, genome-wide analysis of genes that encode core members of the soybean UBS in this study. A total of 1431 genes were identified with high confidence to encode putative soybean UBS components, including 4 genes encoding E1s, 71 genes that encode the E2s, and 1356 genes encoding the E3-related components. Among the E3-encoding genes, 760 encode RING-type E3s, 124 encode U-box domain-containing E3s, and 472 encode F-box proteins. To find out whether the identified soybean UBS genes encode active enzymes, a set of genes were randomly selected and the enzymatic activities of their recombinant proteins were tested. Thioester assays indicated proteins encoded by the soybean E1 gene GmUBA1 and the majority of selected E2 genes are active E1 or E2 enzymes, respectively. Meanwhile, most of the purified RING and U-box domain-containing proteins displayed E3 activity in the in vitro ubiquitination assay. In addition, 1034 of the identified soybean UBS genes were found to express in at least one of 14 soybean tissues examined and the transcript level of 338 soybean USB genes were significantly changed after abiotic or biotic (Fusarium oxysporum and Rhizobium strains) stress treatment. Finally, the expression level of a large number of the identified soybean UBS-related genes was found significantly altered after soybean cyst nematode (SCN) treatment, suggesting the soybean UBS potentially plays an important role in soybean immunity against SCN. CONCLUSIONS: Our findings indicate the presence of a large and diverse number of core UBS proteins in the soybean genome, which suggests that target-specific modification by ubiquitin is a complex and important part of cellular and physiological regulation in soybean. We also revealed certain members of the soybean UBS may be involved in immunity against soybean cyst nematode (SCN). This study sets up an essential foundation for further functional characterization of the soybean UBS in various physiological processes, such as host immunity against SCN. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1365-7) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6052599
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-60525992018-07-20 Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode Zhang, Chunyu Song, Li Choudhary, Mani Kant Zhou, Bangjun Sun, Guangchao Broderick, Kyle Giesler, Loren Zeng, Lirong BMC Plant Biol Research Article BACKGROUND: Ubiquitination is a major post-translational protein modification that regulates essentially all cellular and physiological pathways in eukaryotes. The ubiquitination process typically involves three distinct classes of enzymes, ubiquitin-activating enzyme (E1), ubiquitin-conjugating enzyme (E2) and ubiquitin ligase (E3). To date, a comprehensive identification and analysis of core components comprising of the whole soybean (Glycine max) ubiquitin system (UBS) has not been reported. RESULTS: We performed a systematic, genome-wide analysis of genes that encode core members of the soybean UBS in this study. A total of 1431 genes were identified with high confidence to encode putative soybean UBS components, including 4 genes encoding E1s, 71 genes that encode the E2s, and 1356 genes encoding the E3-related components. Among the E3-encoding genes, 760 encode RING-type E3s, 124 encode U-box domain-containing E3s, and 472 encode F-box proteins. To find out whether the identified soybean UBS genes encode active enzymes, a set of genes were randomly selected and the enzymatic activities of their recombinant proteins were tested. Thioester assays indicated proteins encoded by the soybean E1 gene GmUBA1 and the majority of selected E2 genes are active E1 or E2 enzymes, respectively. Meanwhile, most of the purified RING and U-box domain-containing proteins displayed E3 activity in the in vitro ubiquitination assay. In addition, 1034 of the identified soybean UBS genes were found to express in at least one of 14 soybean tissues examined and the transcript level of 338 soybean USB genes were significantly changed after abiotic or biotic (Fusarium oxysporum and Rhizobium strains) stress treatment. Finally, the expression level of a large number of the identified soybean UBS-related genes was found significantly altered after soybean cyst nematode (SCN) treatment, suggesting the soybean UBS potentially plays an important role in soybean immunity against SCN. CONCLUSIONS: Our findings indicate the presence of a large and diverse number of core UBS proteins in the soybean genome, which suggests that target-specific modification by ubiquitin is a complex and important part of cellular and physiological regulation in soybean. We also revealed certain members of the soybean UBS may be involved in immunity against soybean cyst nematode (SCN). This study sets up an essential foundation for further functional characterization of the soybean UBS in various physiological processes, such as host immunity against SCN. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1365-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-18 /pmc/articles/PMC6052599/ /pubmed/30021519 http://dx.doi.org/10.1186/s12870-018-1365-7 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Zhang, Chunyu
Song, Li
Choudhary, Mani Kant
Zhou, Bangjun
Sun, Guangchao
Broderick, Kyle
Giesler, Loren
Zeng, Lirong
Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title_full Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title_fullStr Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title_full_unstemmed Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title_short Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
title_sort genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6052599/
https://www.ncbi.nlm.nih.gov/pubmed/30021519
http://dx.doi.org/10.1186/s12870-018-1365-7
work_keys_str_mv AT zhangchunyu genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT songli genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT choudharymanikant genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT zhoubangjun genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT sunguangchao genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT broderickkyle genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT gieslerloren genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode
AT zenglirong genomewideanalysisofgenesencodingcorecomponentsoftheubiquitinsysteminsoybeanglycinemaxrevealsapotentialroleforubiquitinationinhostimmunityagainstsoybeancystnematode