A virus-derived siRNA activates plant immunity by interfering with ROS scavenging

Liu, Peng; Zhang, Xiaoxiang; Zhang, Fan; Xu, Menghui; Ye, Zhuangxin; Wang, Ke; Liu, Shuang; Han, Xiaolei; Cheng, Ye; Zhong, Kaili; Zhang, Tianye; Li, Linzhi; Ma, Yupo; Chen, Ming; Chen, Jianping; Yang, Jian

doi:10.1016/j.molp.2021.03.022

Cited by 40 publications

(41 citation statements)

References 53 publications

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“…Regarding ROS activation, expressions of genes of the ROS scavenger thioredoxin, which mediates virus derived small interfering RNA (vsiRNA) effects on ROS accumulation 18 , were differentially downregulated at both early and late post-recovery stages (Supplementary Table S5 ). In addition, two AO genes were differentially upregulated in the 'early post-recovery stage' BYIs and four AO genes were differentially upregulated in the 'late post-recovery stage' BYIs (supplementary Table S5 ).…”

Section: Resultsmentioning

confidence: 99%

“…The relative expressions of RDR1a and RDR1b that were expressed in healthy plants as well, was not significantly different between the BYIs and the associated dark green surrounding tissue. Concomitant upregulation of endoribonuclease Dicer homolog 1 and AGO 1, as well as downregulation of thioredoxin, responsive to vsiRNAs 18 , could indicate JA activation of RNA silencing in the BYIs at that early disease stage 14 . In addition, the early thioredoxin downregulation and AO upregulation that could lead to ROS accumulation as well as the associated activation of plant immunity and antiviral response 35 (Supplementary Tables S3 , S5 ) could affirm the importance of the infectious CGMMV, localized in the 'early post-recovery stage' BYIs, to CGMMV systemic infection (Table 1 ).…”

Section: Discussionmentioning

confidence: 99%

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New early phenotypic markers for cucumber green mottle mosaic virus disease in cucumbers exposed to fluctuating extreme temperatures

Molad

Smith

Luria

et al. 2021

Sci Rep

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Studies of early stages of cucumber green mottle mosaic virus (CGMMV) disease have been recently focused on plant molecular responses. However, extreme diurnal environmental temperatures, characteristic of global climate changes, could affect plant susceptibility and disease phenotype progression. Our studies of CGMMV disease progression, under simulated extreme temperature waves, have revealed two new disease initiation phenotypes that developed gradually, preceding severe symptom manifestations of post-recovery CGMMV systemic infections. 'Early post-recovery stage' bright yellow islands (BYIs) with defined boundaries amid asymptomatic leaf blades were first emerging followed by 'late post-recovery stage' BYIs with diffused boundaries. A deduced CGMMV disease progression scheme, postulating BYI symptom occurrence time-windows, revealed BYIs in field grown cucumber plants exposed to extreme diurnal temperatures. Profiling ontology of cucumber differentially expressed genes in BYIs vs the associated dark-green surrounding tissues disclosed activation of jasmonic acid (JA) pathway in 'early post-recovery stage' BYIs. JA signaling was inactivated in 'late post-recovery stage' BYIs concomitant with increasing expressions of JA signaling inhibitors and downregulation of JA responsive phenylpropanoid pathway. Our results disclosed a new phenotypic description of CGMMV disease initiation, characteristic of cucumbers grown under extreme environmental temperature fluctuations. The BYI phenotypes could define a time-window for CGMMV disease management applications.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

New early phenotypic markers for cucumber green mottle mosaic virus disease in cucumbers exposed to fluctuating extreme temperatures

Molad

Smith

Luria

et al. 2021

Sci Rep

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“…Under developmentally senescence and dark-induced senescence condition, the SGRi leaves show a stay-green phenotype, while under heat stress condition, the SGRi leaves show an accelerated or rapid senescence phenotype. This model was drawn with reference to Aubry et al (2020), Liu et al (2021), and Sakuraba et al (2014).…”

Section: Discussionmentioning

confidence: 99%

STAYGREEN-mediated chlorophyll a catabolism is critical for photosystem stability upon heat stress in ryegrass

Zhang

Huang

et al. 2021

Preprint

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Chlorophyll (Chl) loss is one of the most visible symptoms of heat-induced leaf senescence, especially for cool-season grass species. Suppression of the Chl a Me-dechelatase gene, SGR (also named as nye1), blocked the degradation of Chl a and resulted in the 'stay-green' trait during leaf senescence. However, effect of Chl a catabolism on plant tolerance to long-term moderate heat stress (35-40?) remains unclear. In this study, we suppressed the expression of Chl a catabolic gene, LpSGR, in both constitutive and inducible manners in perennial ryegrass. Constitutive suppression of LpSGR aggravated heat stress-induced chloroplast structure and photosystem damages, disrupted energy utilization/dissipation during photosynthesis, activated ROS generation with weakened ROS-scavenging enzyme activities. Transcriptome comparison among wildtype (WT) and transgenic RNAi plants under either the optimum or high temperature conditions also emphasized the effect of Chl a catabolism on expression of genes encoding photosynthesis system, ROS-generation and scavenging system, and heat shock transcription factors. Furthermore, making use of a modified ethanol-inducible system, we generated stable transgenic perennial ryegrass to suppress LpSGR in an inducible manner. Without ethanol induction, these transgenic lines exhibited the same growth and heat tolerance traits to WT, while under the induction of ethanol spray, the transgenic lines also showed compromised heat tolerance. Taken together, our data suggest that Chl a catabolism is critical for energy dissipation and electron transfer in photosynthesis, ROS-balancing and chloroplast membrane system stability upon long-term moderate heat stress.

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“…Upon incorporation into the RISC, the vsiRNAs suppress the expression of TaAAED1 in a dose-dependent (more viral RNA, more downregulation) and sequence-specific manner. Therefore, chloroplast-generated ROS are known to induce retrograde signalling (from the chloroplast to the nucleus), leading to the modulation of the expression of pathogenesis-related genes that are involved in the defense response to viruses [ 79 ].…”

Section: Main Textmentioning

confidence: 99%

Regulation of plant antiviral defense genes via host RNA-silencing mechanisms

Leonetti

Stuttmann

Pantaleo

2021

Virol J

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Background Plants in nature or crops in the field interact with a multitude of beneficial or parasitic organisms, including bacteria, fungi and viruses. Viruses are highly specialized to infect a limited range of host plants, leading in extreme cases to the full invasion of the host and a diseased phenotype. Resistance to viruses can be mediated by various passive or active mechanisms, including the RNA-silencing machinery and the innate immune system. Main text RNA-silencing mechanisms may inhibit viral replication, while viral components can elicit the innate immune system. Viruses that successfully enter the plant cell can elicit pattern-triggered immunity (PTI), albeit by yet unknown mechanisms. As a counter defense, viruses suppress PTI. Furthermore, viral Avirulence proteins (Avr) may be detected by intracellular immune receptors (Resistance proteins) to elicit effector-triggered immunity (ETI). ETI often culminates in a localized programmed cell death reaction, the hypersensitive response (HR), and is accompanied by a potent systemic defense response. In a dichotomous view, RNA silencing and innate immunity are seen as two separate mechanisms of resistance. Here, we review the intricate connections and similarities between these two regulatory systems, which are collectively required to ensure plant fitness and resilience. Conclusions The detailed understanding of immune regulation at the transcriptional level provides novel opportunities for enhancing plant resistance to viruses by RNA-based technologies. However, extensive use of RNA technologies requires a thorough understanding of the molecular mechanisms of RNA gene regulation. We describe the main examples of host RNA-mediated regulation of virus resistance.

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A virus-derived siRNA activates plant immunity by interfering with ROS scavenging

Cited by 40 publications

References 53 publications

New early phenotypic markers for cucumber green mottle mosaic virus disease in cucumbers exposed to fluctuating extreme temperatures

New early phenotypic markers for cucumber green mottle mosaic virus disease in cucumbers exposed to fluctuating extreme temperatures

STAYGREEN-mediated chlorophyll a catabolism is critical for photosystem stability upon heat stress in ryegrass

Regulation of plant antiviral defense genes via host RNA-silencing mechanisms

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