Photosynthesis‐related genes induce resistance against soybean mosaic virus: Evidence for involvement of the RNA silencing pathway

Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance g...

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Published inMolecular plant pathology Vol. 23; no. 4; pp. 543 - 560
Main Authors Bwalya, John, Alazem, Mazen, Kim, Kook‐Hyung
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.04.2022
John Wiley and Sons Inc
Subjects
Adenosine Triphosphate - metabolism
ATPsyn‐α
avirulent strains
Biosynthesis
Chimeras
Chloroplasts
Coronaviruses
Cultivars
Cytochrome
Cytoplasm
Disease resistance
Flowers & plants
Gene expression
Gene silencing
Genes
Genomes
Glycine max
Hormones
Hormones - metabolism
immunity
Infections
Nicotiana benthamiana
Original
Permeability
Photosynthesis
Photosynthesis - genetics
Photosystem I
Plant Diseases
plant hormones
Plant immunity
plant pathology
plant–virus interactions
Potyvirus
Proteins
PSaC
PsaC gene
resistance genes
Ribonucleic acid
RNA
RNA Interference
RNA silencing
RNA-mediated interference
Salicylic acid
sequence analysis
soybean
Soybean mosaic virus
Soybeans
Viral infections
Virulence
virulent strains
Viruses
PSaC
soybean
photosynthesis
plant-virus interactions
ATPsyn-α
plant hormones
RNA silencing
soybean mosaic virus
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Abstract Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance gene, showed that several chloroplast‐related genes were strongly induced in response to infection with an avirulent strain of soybean mosaic virus (SMV), G5H, but were weakly induced in response to a virulent strain, G7H. For further analysis, we selected the PSaC gene from the photosystem I and the ATP‐synthase α‐subunit (ATPsyn‐α) gene whose encoded protein is part of the ATP‐synthase complex. Overexpression of either gene within the G7H genome reduced virus levels in the susceptible cultivar Lee74 (rsv3‐null). This result was confirmed by transiently expressing both genes in Nicotiana benthamiana followed by G7H infection. Both proteins localized in the chloroplast envelope as well as in the nucleus and cytoplasm. Because the chloroplast is the initial biosynthesis site of defence‐related hormones, we determined whether hormone‐related genes are involved in the ATPsyn‐α‐ and PSaC‐mediated defence. Interestingly, genes involved in the biosynthesis of several hormones were up‐regulated in plants infected with SMV‐G7H expressing ATPsyn‐α. However, only jasmonic and salicylic acid biosynthesis genes were up‐regulated following infection with the SMV‐G7H expressing PSaC. Both chimeras induced the expression of several antiviral RNA silencing genes, which indicate that such resistance may be partially achieved through the RNA silencing pathway. These findings highlight the role of photosynthesis‐related genes in regulating resistance to viruses. Two photosynthesis‐related genes, PSaC and ATPsyn‐α, contribute to resistance against soybean mosaic virus via the RNA silencing pathway.
AbstractList Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance gene, showed that several chloroplast‐related genes were strongly induced in response to infection with an avirulent strain of soybean mosaic virus (SMV), G5H, but were weakly induced in response to a virulent strain, G7H. For further analysis, we selected the PSaC gene from the photosystem I and the ATP‐synthase α‐subunit (ATPsyn‐α) gene whose encoded protein is part of the ATP‐synthase complex. Overexpression of either gene within the G7H genome reduced virus levels in the susceptible cultivar Lee74 (rsv3‐null). This result was confirmed by transiently expressing both genes in Nicotiana benthamiana followed by G7H infection. Both proteins localized in the chloroplast envelope as well as in the nucleus and cytoplasm. Because the chloroplast is the initial biosynthesis site of defence‐related hormones, we determined whether hormone‐related genes are involved in the ATPsyn‐α‐ and PSaC‐mediated defence. Interestingly, genes involved in the biosynthesis of several hormones were up‐regulated in plants infected with SMV‐G7H expressing ATPsyn‐α. However, only jasmonic and salicylic acid biosynthesis genes were up‐regulated following infection with the SMV‐G7H expressing PSaC. Both chimeras induced the expression of several antiviral RNA silencing genes, which indicate that such resistance may be partially achieved through the RNA silencing pathway. These findings highlight the role of photosynthesis‐related genes in regulating resistance to viruses. Two photosynthesis‐related genes, PSaC and ATPsyn‐α, contribute to resistance against soybean mosaic virus via the RNA silencing pathway.
Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance gene, showed that several chloroplast‐related genes were strongly induced in response to infection with an avirulent strain of soybean mosaic virus (SMV), G5H, but were weakly induced in response to a virulent strain, G7H. For further analysis, we selected the PSaC gene from the photosystem I and the ATP‐synthase α‐subunit ( ATPsyn‐α ) gene whose encoded protein is part of the ATP‐synthase complex. Overexpression of either gene within the G7H genome reduced virus levels in the susceptible cultivar Lee74 ( rsv3 ‐null). This result was confirmed by transiently expressing both genes in Nicotiana benthamiana followed by G7H infection. Both proteins localized in the chloroplast envelope as well as in the nucleus and cytoplasm. Because the chloroplast is the initial biosynthesis site of defence‐related hormones, we determined whether hormone‐related genes are involved in the ATPsyn‐α‐ and PSaC‐ mediated defence. Interestingly, genes involved in the biosynthesis of several hormones were up‐regulated in plants infected with SMV‐G7H expressing ATPsyn‐α. However, only jasmonic and salicylic acid biosynthesis genes were up‐regulated following infection with the SMV‐G7H expressing PSaC. Both chimeras induced the expression of several antiviral RNA silencing genes, which indicate that such resistance may be partially achieved through the RNA silencing pathway. These findings highlight the role of photosynthesis‐related genes in regulating resistance to viruses.
Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance gene, showed that several chloroplast‐related genes were strongly induced in response to infection with an avirulent strain of soybean mosaic virus (SMV), G5H, but were weakly induced in response to a virulent strain, G7H. For further analysis, we selected the PSaC gene from the photosystem I and the ATP‐synthase α‐subunit (ATPsyn‐α) gene whose encoded protein is part of the ATP‐synthase complex. Overexpression of either gene within the G7H genome reduced virus levels in the susceptible cultivar Lee74 (rsv3‐null). This result was confirmed by transiently expressing both genes in Nicotiana benthamiana followed by G7H infection. Both proteins localized in the chloroplast envelope as well as in the nucleus and cytoplasm. Because the chloroplast is the initial biosynthesis site of defence‐related hormones, we determined whether hormone‐related genes are involved in the ATPsyn‐α‐ and PSaC‐mediated defence. Interestingly, genes involved in the biosynthesis of several hormones were up‐regulated in plants infected with SMV‐G7H expressing ATPsyn‐α. However, only jasmonic and salicylic acid biosynthesis genes were up‐regulated following infection with the SMV‐G7H expressing PSaC. Both chimeras induced the expression of several antiviral RNA silencing genes, which indicate that such resistance may be partially achieved through the RNA silencing pathway. These findings highlight the role of photosynthesis‐related genes in regulating resistance to viruses.
Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of photosynthesis‐related genes in plant immunity is largely unexplored. Analysis of RNA‐Seq data from the soybean cultivar L29, which carries the Rsv3 resistance gene, showed that several chloroplast‐related genes were strongly induced in response to infection with an avirulent strain of soybean mosaic virus (SMV), G5H, but were weakly induced in response to a virulent strain, G7H. For further analysis, we selected the PSaC gene from the photosystem I and the ATP‐synthase α‐subunit ( ATPsyn‐α ) gene whose encoded protein is part of the ATP‐synthase complex. Overexpression of either gene within the G7H genome reduced virus levels in the susceptible cultivar Lee74 ( rsv3 ‐null). This result was confirmed by transiently expressing both genes in Nicotiana benthamiana followed by G7H infection. Both proteins localized in the chloroplast envelope as well as in the nucleus and cytoplasm. Because the chloroplast is the initial biosynthesis site of defence‐related hormones, we determined whether hormone‐related genes are involved in the ATPsyn‐α‐ and PSaC‐ mediated defence. Interestingly, genes involved in the biosynthesis of several hormones were up‐regulated in plants infected with SMV‐G7H expressing ATPsyn‐α. However, only jasmonic and salicylic acid biosynthesis genes were up‐regulated following infection with the SMV‐G7H expressing PSaC. Both chimeras induced the expression of several antiviral RNA silencing genes, which indicate that such resistance may be partially achieved through the RNA silencing pathway. These findings highlight the role of photosynthesis‐related genes in regulating resistance to viruses. Two photosynthesis‐related genes, PS aC and ATPsyn‐α , contribute to resistance against soybean mosaic virus via the RNA silencing pathway.
Author Alazem, Mazen
Kim, Kook‐Hyung
Bwalya, John
AuthorAffiliation 1 Department of Agriculture Biotechnology College of Agriculture and Life Sciences Seoul National University Seoul Republic of Korea
3 Research of Institute Agriculture and Life Sciences Seoul National University Seoul Republic of Korea
2 Plant Genomics and Breeding Institute Seoul National University Seoul Republic of Korea
AuthorAffiliation_xml – name: 3 Research of Institute Agriculture and Life Sciences Seoul National University Seoul Republic of Korea
– name: 1 Department of Agriculture Biotechnology College of Agriculture and Life Sciences Seoul National University Seoul Republic of Korea
– name: 2 Plant Genomics and Breeding Institute Seoul National University Seoul Republic of Korea
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  surname: Bwalya
  fullname: Bwalya, John
  organization: Seoul National University
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  givenname: Mazen
  orcidid: 0000-0003-3690-7459
  surname: Alazem
  fullname: Alazem, Mazen
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  organization: Seoul National University
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  givenname: Kook‐Hyung
  orcidid: 0000-0001-9066-6903
  surname: Kim
  fullname: Kim, Kook‐Hyung
  email: kookkim@snu.ac.kr
  organization: Seoul National University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34962034$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords PSaC
soybean
photosynthesis
plant-virus interactions
ATPsyn-α
plant hormones
RNA silencing
soybean mosaic virus
Language English
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PublicationTitle Molecular plant pathology
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PublicationYear 2022
Publisher John Wiley & Sons, Inc
John Wiley and Sons Inc
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Snippet Increasing lines of evidence indicate that chloroplast‐related genes are involved in plant–virus interactions. However, the involvement of...
Increasing lines of evidence indicate that chloroplast-related genes are involved in plant-virus interactions. However, the involvement of...
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SubjectTerms Adenosine Triphosphate - metabolism
ATPsyn‐α
avirulent strains
Biosynthesis
Chimeras
Chloroplasts
Coronaviruses
Cultivars
Cytochrome
Cytoplasm
Disease resistance
Flowers & plants
Gene expression
Gene silencing
Genes
Genomes
Glycine max
Hormones
Hormones - metabolism
immunity
Infections
Nicotiana benthamiana
Original
Permeability
Photosynthesis
Photosynthesis - genetics
Photosystem I
Plant Diseases
plant hormones
Plant immunity
plant pathology
plant–virus interactions
Potyvirus
Proteins
PSaC
PsaC gene
resistance genes
Ribonucleic acid
RNA
RNA Interference
RNA silencing
RNA-mediated interference
Salicylic acid
sequence analysis
soybean
Soybean mosaic virus
Soybeans
Viral infections
Virulence
virulent strains
Viruses
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Title Photosynthesis‐related genes induce resistance against soybean mosaic virus: Evidence for involvement of the RNA silencing pathway
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Volume 23
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