Geminiviruses boost active DNA demethylation for counter-defense

Guo, Yushuang; Jia, Mengao; Li, Shaofang; Li, Fangfang

doi:10.1016/j.tim.2022.02.002

Cited by 10 publications

(7 citation statements)

References 10 publications

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“…During the ongoing tug of plants and viruses, plants mount various highly conserved defense mechanisms against virus infection, and viruses have evolved counteracting strategies for their adaption (Li and Wang, 2019; Yang et al, 2020; Guo et al, 2022). Emerging evidence indicates that autophagy has co‐evolved into a double‐edged sword on the battlefields between plants and viruses (Hofius et al, 2017; Kushwaha et al, 2019; Yang et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Geminiviral C2 proteins inhibit active autophagy to facilitate virus infection by impairing the interaction of ATG7 and ATG8

Cao

Zhang

et al. 2023

JIPB

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Autophagy is a conserved intracellular degradation process that plays an active role in plant response to virus infections. Here we report that geminiviruses counteract activated autophagymediated antiviral defense in plant cells through the C2 proteins they encode. We found that, in Nicotiana benthamiana plants, tomato leaf curl Yunnan virus (TLCYnV) infection upregulated the transcription levels of autophagy-related genes (ATGs). Overexpression of NbATG5, NbATG7, or NbATG8a in N. benthamiana plants decreased TLCYnV accumulation and attenuated viral symptoms. Interestingly, transgenic overexpression of NbATG7 promoted the growth of N. benthamiana plants and enhanced plant resistance to TLCYnV. We further revealed that the C2 protein encoded by TLCYnV directly interacted with the ubiquitinactivating domain of ATG7. This interaction competitively disrupted the ATG7-ATG8 binding in N. benthamiana and Solanum lycopersicum plants, thereby inhibiting autophagy activity. Furthermore, we uncovered that the C2-mediated autophagy inhibition mechanism was conserved in three other geminiviruses. In summary, we discovered a novel counter-defensive strategy employed by geminiviruses that enlists their C2 proteins as disrupters of ATG7-ATG8 interactions to defeat antiviral autophagy.

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Section: Discussionmentioning

confidence: 99%

Geminiviral C2 proteins inhibit active autophagy to facilitate virus infection by impairing the interaction of ATG7 and ATG8

Cao

Zhang

et al. 2023

JIPB

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“…Suppression of TGS alters the methylation status of the host genome as well as viral DNA ( Gui et al., 2022 ; Zhang et al., 2023 ). Begomovirus infection has been associated with demethylation and activation of transposable elements in the host genome ( Gui et al., 2022 ; Guo et al., 2022 ) and similarly might activate the genomic copy of SEGS-1 in cassava. The efficiency of SEGS-1 activation may be affected by many factors including cassava genetic variation, CMB virulence, disease pressure, and environmental conditions ( Legg et al., 2015 ; Ferguson et al., 2019 ; Houngue et al., 2019 ; Patil and Fauquet, 2021 ), such that SEGS-1 is activated in some but not all cassava plants during infection.…”

Section: Discussionmentioning

confidence: 99%

SEGS-1 a cassava genomic sequence increases the severity of African cassava mosaic virus infection in Arabidopsis thaliana

Rajabu,

Dallas,

Chiunga

et al. 2023

Front. Plant Sci.

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Cassava is a major crop in Sub-Saharan Africa, where it is grown primarily by smallholder farmers. Cassava production is constrained by Cassava mosaic disease (CMD), which is caused by a complex of cassava mosaic begomoviruses (CMBs). A previous study showed that SEGS-1 (sequences enhancing geminivirus symptoms), which occurs in the cassava genome and as episomes during viral infection, enhances CMD symptoms and breaks resistance in cassava. We report here that SEGS-1 also increases viral disease severity in Arabidopsis thaliana plants that are co-inoculated with African cassava mosaic virus (ACMV) and SEGS-1 sequences. Viral disease was also enhanced in Arabidopsis plants carrying a SEGS-1 transgene when inoculated with ACMV alone. Unlike cassava, no SEGS-1 episomal DNA was detected in the transgenic Arabidopsis plants during ACMV infection. Studies using Nicotiana tabacum suspension cells showed that co-transfection of SEGS-1 sequences with an ACMV replicon increases viral DNA accumulation in the absence of viral movement. Together, these results demonstrated that SEGS-1 can function in a heterologous host to increase disease severity. Moreover, SEGS-1 is active in a host genomic context, indicating that SEGS-1 episomes are not required for disease enhancement.

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“…The inhibition of DNA methylation by viral proteins Geminiviruses co-opt multiple viral proteins to escape methylation by either regulating host proteins in the DNA methylation pathways or suppressing the generation of the methyl group donor SAM. Almost every positional ortholog of geminiviral proteins can perturb the DNA methylation pathway through various strategies (Guo et al, 2022). For example, the expression of a geminivirus C5 protein inhibits the Domains Rearranged Methyltransferase 2 transcription (Li et al, 2015a).…”

Section: Antiviral Defense and Viral Counter-defense In Plants At The...mentioning

confidence: 99%

“…In contrast to the DNA methylation reaction, active DNA demethylation requires DNA demethylases. Although the mechanism by which geminivirus-derived small interfering RNAs (siRNAs) trigger RdDM remains largely obscure, many studies have shown that geminivirus DNA is methylated in infected plants and that reduced cytosine methylation in the viral genome promotes viral pathogenicity (Guo et al, 2022). Consistently, plants with deficiencies in establishing or maintaining DNA methylation are hypersusceptible to geminiviruses and display exacerbated disease symptoms with higher viral DNA accumulations, and vice versa (Yang et al, 2011).…”

Section: Antiviral Defense and Viral Counter-defense In Plants At The...mentioning

confidence: 99%

Plant virology in the 21st century in China: Recent advances and future directions

Wu,

Zhang,

et al. 2024

JIPB

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Plant viruses are a group of intracellular pathogens that persistently threaten global food security. Significant advances in plant virology have been achieved by Chinese scientists over the last 20 years, including basic research and technologies for preventing and controlling plant viral diseases. Here, we review these milestones and advances, including the identification of new crop‐infecting viruses, dissection of pathogenic mechanisms of multiple viruses, examination of multilayered interactions among viruses, their host plants, and virus‐transmitting arthropod vectors, and in‐depth interrogation of plant‐encoded resistance and susceptibility determinants. Notably, various plant virus‐based vectors have also been successfully developed for gene function studies and target gene expression in plants. We also recommend future plant virology studies in China.This article is protected by copyright. All rights reserved.

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Geminiviruses boost active DNA demethylation for counter-defense

Cited by 10 publications

References 10 publications

Geminiviral C2 proteins inhibit active autophagy to facilitate virus infection by impairing the interaction of ATG7 and ATG8

Geminiviral C2 proteins inhibit active autophagy to facilitate virus infection by impairing the interaction of ATG7 and ATG8

SEGS-1 a cassava genomic sequence increases the severity of African cassava mosaic virus infection in Arabidopsis thaliana

Plant virology in the 21st century in China: Recent advances and future directions

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