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

Chunyu Zhang, Li Song, Mani Kant Choudhary, Bangjun Zhou, Guangchao Sun, Kyle Broderick, Loren Giesler, Lirong Zeng

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

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 coreUBS 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 invarious physiological processes, such ashost immunity against SCN.

Original languageEnglish (US)
Article number149
JournalBMC plant biology
Volume18
Issue number1
DOIs
StatePublished - Jul 18 2018

Fingerprint

Heterodera glycines
ubiquitin
Glycine max
immunity
soybeans
genome
genes
ubiquitin-protein ligase
ubiquitination
enzymes
F-box proteins
physiological regulation
proteins
assays
Fusarium oxysporum
soy protein
recombinant proteins
Rhizobium
eukaryotic cells

Keywords

  • F-box domain
  • Immunity
  • RING domain
  • Soybean
  • Soybean cyst nematode
  • U-box domain
  • Ubiquitin system (UBS)
  • Ubiquitin-activating enzyme (E1)
  • Ubiquitin-conjugating enzyme (E2)

ASJC Scopus subject areas

  • Plant Science

Cite this

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.

In: BMC plant biology, Vol. 18, No. 1, 149, 18.07.2018.

Research output: Contribution to journalArticle

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abstract = "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 coreUBS 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 invarious physiological processes, such ashost immunity against SCN.",
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AU - Song, Li

AU - Choudhary, Mani Kant

AU - Zhou, Bangjun

AU - Sun, Guangchao

AU - Broderick, Kyle

AU - Giesler, Loren

AU - Zeng, Lirong

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KW - Soybean cyst nematode

KW - U-box domain

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KW - Ubiquitin-activating enzyme (E1)

KW - Ubiquitin-conjugating enzyme (E2)

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