Identification of differentially regulated maize proteins conditioning Sugarcane mosaic virus systemic infection

Abstract

Sugarcane mosaic virus (SCMV) is the most important cause of maize dwarf mosaic disease. To identify maize genes responsive to SCMV infection and that may be involved in pathogenesis, a comparative proteomic analysis was performed using the first and second systemically infected leaves (termed 1 SL and 2 SL, respectively). Seventy-one differentially expressed proteins were identified in 1 SL and 2 SL upon SCMV infection. Among them, eight proteins showed the same changing patterns in both 1 SL and 2 SL. Functional annotations of regulated proteins and measurement of photosynthetic activity revealed that photosynthesis was more inhibited and defensive gene expression more pronounced in 1 SL than in 2 SL. Knockdown of regulated proteins in both 1 SL and 2 SL by a brome mosaic virus-based gene silencing vector in maize indicated that protein disulfide isomerase-like and phosphoglycerate kinase were required for optimal SCMV replication. By contrast, knockdown of polyamine oxidase (ZmPAO) significantly increased SCMV accumulation, implying that ZmPAO activity might contribute to resistance or tolerance. The results suggest that combining comparative proteomic analyses of different tissues and virus-induced gene silencing is an efficient way to identify host proteins supporting virus replication or enhancing resistance to virus infection.

Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

“…To investigate whether immunity response correlated with enhanced SCMV infection by lactate treatment, we measured the expression levels of the pathogenesis-related ( PR ) genes and the accumulation of H 2 O 2 in SCMV-infected maize leaves at 24 h post lactate or water treatment. As previously reported ( Chen et al., 2017a ; Yuan et al., 2019 ), SCMV infection stimulated the expression levels of PR genes ( ZmPR1 , ZmPR3 , ZmPR4 and ZmPR5 ) and the accumulation levels of H 2 O 2 ( Figure 7F ). Intriguingly, lactate treatment significantly decreased the expression levels of PR genes in SCMV-infected plants ( Figure 7 ).…”

“…Previous studies found that maize plants mainly showed systemically mosaic symptoms at 5 dpi of SCMV ( Chen et al., 2017a ; Chen et al., 2017b ; Du et al., 2020 ). In this study, we also discovered that only 1.3% of maize plants (3 of 221-inoculated plants in three replicates) started to show mosaic symptoms at 4 dpi, whereas almost all SCMV-infected maize plants developed mosaic symptoms on the first systemically infected leaf (referred to as 1 SL) at 5 dpi ( Figure 1 and Supplementary Figure 1 ).…”

Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

“…To investigate whether immunity response correlated with enhanced SCMV infection by lactate treatment, we measured the expression levels of the pathogenesis-related ( PR ) genes and the accumulation of H 2 O 2 in SCMV-infected maize leaves at 24 h post lactate or water treatment. As previously reported ( Chen et al., 2017a ; Yuan et al., 2019 ), SCMV infection stimulated the expression levels of PR genes ( ZmPR1 , ZmPR3 , ZmPR4 and ZmPR5 ) and the accumulation levels of H 2 O 2 ( Figure 7F ). Intriguingly, lactate treatment significantly decreased the expression levels of PR genes in SCMV-infected plants ( Figure 7 ).…”

“…Previous studies found that maize plants mainly showed systemically mosaic symptoms at 5 dpi of SCMV ( Chen et al., 2017a ; Chen et al., 2017b ; Du et al., 2020 ). In this study, we also discovered that only 1.3% of maize plants (3 of 221-inoculated plants in three replicates) started to show mosaic symptoms at 4 dpi, whereas almost all SCMV-infected maize plants developed mosaic symptoms on the first systemically infected leaf (referred to as 1 SL) at 5 dpi ( Figure 1 and Supplementary Figure 1 ).…”

Advances in research on maize lethal necrosis, a devastating viral disease

“…Therefore, eIF4E may be a potential target for engineering resistance to MLN. Similar to the results obtained during the roles of eIF4E in MCMV/SCMV infection, protein disulfide isomerase (PDI) was also reported to support both MCMV and SCMV accumulation (Chen et al 2017a;Dang et al 2020). However, the roles of host factors in MCMV and/or SCMV infection are not always the same.…”

Proteomic Changes during MCMV Infection Revealed by iTRAQ Quantitative Proteomic Analysis in Maize

“…In addition, a PDI-like protein HvPDIL5-1 derived from barley was confirmed to function as a susceptibility factor to bymoviruses infection [63]. Similarly, the iTRAQ analyses revealed that maize PDIL expression is upregulated in leaf tissues after SCMV infection, and knockdown of PDIL through brome mosaic virus-based VIGS can impair SCMV replication [26]. In the present study, we determined that ZmPDIL-1 was upregulated at both the protein and transcription levels after MCMV infection.…”

Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

“…To investigate whether immunity response correlated with enhanced SCMV infection by lactate treatment, we measured the expression levels of the pathogenesis-related ( PR ) genes and the accumulation of H 2 O 2 in SCMV-infected maize leaves at 24 h post lactate or water treatment. As previously reported ( Chen et al., 2017a ; Yuan et al., 2019 ), SCMV infection stimulated the expression levels of PR genes ( ZmPR1 , ZmPR3 , ZmPR4 and ZmPR5 ) and the accumulation levels of H 2 O 2 ( Figure 7F ). Intriguingly, lactate treatment significantly decreased the expression levels of PR genes in SCMV-infected plants ( Figure 7 ).…”

“…Previous studies found that maize plants mainly showed systemically mosaic symptoms at 5 dpi of SCMV ( Chen et al., 2017a ; Chen et al., 2017b ; Du et al., 2020 ). In this study, we also discovered that only 1.3% of maize plants (3 of 221-inoculated plants in three replicates) started to show mosaic symptoms at 4 dpi, whereas almost all SCMV-infected maize plants developed mosaic symptoms on the first systemically infected leaf (referred to as 1 SL) at 5 dpi ( Figure 1 and Supplementary Figure 1 ).…”

Advances in research on maize lethal necrosis, a devastating viral disease

“…Therefore, eIF4E may be a potential target for engineering resistance to MLN. Similar to the results obtained during the roles of eIF4E in MCMV/SCMV infection, protein disulfide isomerase (PDI) was also reported to support both MCMV and SCMV accumulation (Chen et al 2017a;Dang et al 2020). However, the roles of host factors in MCMV and/or SCMV infection are not always the same.…”

Proteomic Changes during MCMV Infection Revealed by iTRAQ Quantitative Proteomic Analysis in Maize

“…In addition, a PDI-like protein HvPDIL5-1 derived from barley was confirmed to function as a susceptibility factor to bymoviruses infection [63]. Similarly, the iTRAQ analyses revealed that maize PDIL expression is upregulated in leaf tissues after SCMV infection, and knockdown of PDIL through brome mosaic virus-based VIGS can impair SCMV replication [26]. In the present study, we determined that ZmPDIL-1 was upregulated at both the protein and transcription levels after MCMV infection.…”

Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

“…To investigate whether immunity response correlated with enhanced SCMV infection by lactate treatment, we measured the expression levels of the pathogenesis-related ( PR ) genes and the accumulation of H 2 O 2 in SCMV-infected maize leaves at 24 h post lactate or water treatment. As previously reported ( Chen et al., 2017a ; Yuan et al., 2019 ), SCMV infection stimulated the expression levels of PR genes ( ZmPR1 , ZmPR3 , ZmPR4 and ZmPR5 ) and the accumulation levels of H 2 O 2 ( Figure 7F ). Intriguingly, lactate treatment significantly decreased the expression levels of PR genes in SCMV-infected plants ( Figure 7 ).…”

“…Previous studies found that maize plants mainly showed systemically mosaic symptoms at 5 dpi of SCMV ( Chen et al., 2017a ; Chen et al., 2017b ; Du et al., 2020 ). In this study, we also discovered that only 1.3% of maize plants (3 of 221-inoculated plants in three replicates) started to show mosaic symptoms at 4 dpi, whereas almost all SCMV-infected maize plants developed mosaic symptoms on the first systemically infected leaf (referred to as 1 SL) at 5 dpi ( Figure 1 and Supplementary Figure 1 ).…”

Advances in research on maize lethal necrosis, a devastating viral disease

“…Therefore, eIF4E may be a potential target for engineering resistance to MLN. Similar to the results obtained during the roles of eIF4E in MCMV/SCMV infection, protein disulfide isomerase (PDI) was also reported to support both MCMV and SCMV accumulation (Chen et al 2017a;Dang et al 2020). However, the roles of host factors in MCMV and/or SCMV infection are not always the same.…”

Proteomic Changes during MCMV Infection Revealed by iTRAQ Quantitative Proteomic Analysis in Maize

“…In addition, a PDI-like protein HvPDIL5-1 derived from barley was confirmed to function as a susceptibility factor to bymoviruses infection [63]. Similarly, the iTRAQ analyses revealed that maize PDIL expression is upregulated in leaf tissues after SCMV infection, and knockdown of PDIL through brome mosaic virus-based VIGS can impair SCMV replication [26]. In the present study, we determined that ZmPDIL-1 was upregulated at both the protein and transcription levels after MCMV infection.…”