Arabidopsis mutants deficient for ethylene-signaling are hypersensitive to geminivirus infection
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Date
2025-05
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The Ohio State University
Abstract
Geminiviruses are agriculturally important pathogens that are responsible for damaging billions of dollars of crops annually. These viruses package circular single-stranded DNA (ssDNA) in virus particles (virions) and replicate in the host cell nucleus via double-stranded DNA (dsDNA) intermediates that associate with host histones. Because of their small genomes, geminivirus proteins must be multifunctional, including the AL2 and L2 proteins, which are pathogenicity factors encoded by different but related geminiviruses. Critically, AL2/L2 inactivate adenosine kinase (ADK), which, among other roles, is responsible for phosphorylating adenosine to produce adenosine monophosphate (AMP) in the methyl cycle. The methyl cycle generates S-adenosyl methionine (SAM), a methyl group donor and required cofactor for methyltransferases responsible for RNA-directed DNA methylation (RdDM), a key epigenetic defense against geminiviruses. RdDM causes compaction of chromatin, including viral chromatin, which results in transcriptional gene silencing (TGS). When AL2/L2 inactivate ADK, flux through the methyl cycle is inhibited, thereby decreasing SAM synthesis and hindering RdDM. RdDM mutants demonstrate increased susceptibility to geminivirus infection, and AL2/L2 suppression underscores the importance of RdDM as an anti-geminivirus defense. Importantly, SAM is also a biochemical precursor to the gaseous hormone ethylene (Et). Thus, by inhibiting ADK, AL2/L2 might also reduce Et biosynthesis, suggesting Et-signaling may be involved in anti-geminivirus defense. Based on the role SAM plays in RdDM and ethylene biosynthesis, a novel geminivirus mechanism is proposed: the inhibition of the methyl cycle by AL2/L2 hinders multiple antiviral defenses, namely the established RdDM and proposed Et-signaling defenses. In support, we show that AL2/L2 do in fact reduce ethylene biosynthesis. Further, we show that ethylene-insensitive (ein) and ethylene-deficient (acs) Arabidopsis thaliana mutants are hypersensitive to Cabbage leaf curl virus 3 (CaLCuV) and Beet curly top virus (BCTV) infection, with the ethylene-deficient mutant symptoms being especially pronounced. Conversely, ethylene-overproduction mutants demonstrate increased tolerance to geminivirus infection. Moreover, RdDM mutants do not show reduced ethylene production, suggesting that the RdDM and Et-signaling pathways are independent. These findings support RdDM and Et-signaling as distinct anti-geminivirus defense pathways, both of which are inhibited by the inactivation of ADK by AL2/L2.
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Keywords
Geminivirus, Ethylene-signaling, Adenosine kinase (ADK), RNA-directed DNA Methylation (RdDM), AL2/L2