A single viral amino acid shapes the root system architecture of a plant host upon virus infection

Background Grapevine fanleaf virus (GFLV) is one of the most detrimental viral pathogens of grapevines worldwide but no information is available on its effect on the root system architecture (RSA) of plant hosts. We used two wildtype GFLV strains and their single amino acid mutants to assess RSA tra...

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Published in:	BMC microbiology Vol. 24; no. 1; pp. 267 - 20
Main Authors:	Roy, Brandon G., Fuchs, Marc
Format:	Journal Article
Language:	English
Published:	London BioMed Central 19.07.2024 BioMed Central Ltd Springer Nature B.V BMC
Subjects:	Amino acid sequence Amino acids Amino Acids - metabolism Analysis Antiviral agents Antiviral drugs Biological Microscopy Biomass Biomedical and Life Sciences Control Disease transmission DNA-directed RNA polymerase Dosage and administration Gene expression Gene Expression Regulation, Plant Gene silencing Genomes Glycine Hormones Host plants Host-Pathogen Interactions Hypersensitive response Identification and classification Immune response Infection Infections Inoculation Leaves Life Sciences Lysine Microbiology Mutants Mutation Mycology Nepovirus - genetics Nicotiana - genetics Nicotiana - virology Oxygen enrichment Parasitology Pattern analysis Pattern recognition Pattern recognition receptors Phenotype Phenotypes Plant Plant Diseases - genetics Plant Diseases - virology Plant hormones Plant Leaves - genetics Plant Leaves - virology Plant Roots - genetics Plant Roots - virology Plant tissues Plant viruses Plants and Their Pathogens Proteins Reactive oxygen species Receptors Ribonucleic acid RNA RNA polymerase RNA sequencing RNA-directed RNA polymerase RNA-mediated interference Root architecture Roots Symptoms Transcriptome Transcriptomes Transcriptomics Viral infections Viral Proteins - genetics Viral Proteins - metabolism Virology Virus Virus diseases of plants Viruses Vitis - genetics Vitis - virology United States Virus Infection Plant Phenotype Reactive oxygen species Immune response Root architecture Symptoms
ISSN:	1471-2180, 1471-2180
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Summary:	Background Grapevine fanleaf virus (GFLV) is one of the most detrimental viral pathogens of grapevines worldwide but no information is available on its effect on the root system architecture (RSA) of plant hosts. We used two wildtype GFLV strains and their single amino acid mutants to assess RSA traits in infected Nicotiana benthamiana and evaluate transcriptomic changes in host root gene expression in replicated time course 3’RNA-Seq experiments. Mutations targeted the multi-functional GFLV-encoded protein 1E Pol/Sd , a putative RNA-dependent RNA polymerase and determinant of foliar symptoms in N. benthamiana plants. Results Plant infection with wildtype GFLV strain GHu and mutant GFLV strain F13 1E Pol G802K , both carrying a lysine in position 802 of protein 1E Pol/Sd , resulted in a significantly lower number of root tips (-30%), and a significantly increased average root diameter (+ 20%) at 17 days post inoculation (dpi) in comparison with roots of mock inoculated plants. In contrast, the RSA of plants infected with wildtype GFLV strain F13 and mutant GFLV strain GHu 1E Pol K802G , both carrying a glycine in position 802 of protein 1E Pol/Sd , resembled that of mock inoculated plants. Modifications of RSA traits were not associated with GFLV titer. Root tissue transcriptome analysis at 17 dpi indicated dysregulation of pattern recognition receptors, plant hormones, RNA silencing, and genes related to the production of reactive oxygen species (ROS). For wildtype GFLV strain GHu, RSA modifications were correlated with an abundant accumulation of ROS in the pericycle of primary roots at 7 dpi and the duration of vein clearing symptom expression in apical leaves. Dysegulation of a hypersensitive response was an overarching gene ontology found through enrichment analyses of 3’RNA-Seq data. Conclusions Our findings revealed the causative role of lysine in position 802 of protein 1E Pol/Sd in a novel RSA phenotype during viral infection and documented GFLV- N. benthamiana interactions at the root level based on (i) antiviral response, (ii) receptor mediated production of ROS, and (iii) hormone regulation. A correlation between above and below ground symptoms was reported for the first time in plants infected with wildtype GFLV strain GHu. Further work is warranted to test whether the modified RSA of a plant host might impact GFLV acquisition and transmission by the ectoparasitic dagger nematode Xiphinema index .
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23
ISSN:	1471-2180 1471-2180
DOI:	10.1186/s12866-024-03399-x