The Identity of a Single Residue of the RNA-Dependent RNA Polymerase of Grapevine Fanleaf Virus Modulates Vein Clearing in Nicotiana benthamiana

Author:

Osterbaan Larissa J.1ORCID,Choi Jiyeong1,Kenney Jaimie1,Flasco Madison1,Vigne Emmanuelle2,Schmitt-Keichinger Corinne2,Rebelo Ana Rita3,Heck Michelle345,Fuchs Marc1

Affiliation:

1. Cornell University, Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell AgriTech at the New York State Agricultural Experiment Station, Geneva, NY 14456, U.S.A.

2. UMR 1131 Santé de la Vigne et Qualité du Vin, INRA-Université de Strasbourg, 68000 Colmar, France

3. Emerging Pests and Pathogens Research Unit, USDA Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, NY, U.S.A.

4. Boyce Thompson Research Institute for Plant Research, 533 Tower Road, Ithaca, NY 14853, U.S.A.

5. Cornell University, Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, U.S.A.

Abstract

The mechanisms underlying host plant symptom development upon infection by viruses of the genus Nepovirus in the family Secoviridae, including grapevine fanleaf virus (GFLV), are poorly understood. In the systemic host Nicotiana benthamiana, GFLV strain GHu produces characteristic symptoms of vein clearing in apical leaves, unlike other GFLV strains such as F13, which cause an asymptomatic infection. In this study, we expanded on earlier findings and used reverse genetics to identify residue 802 (lysine, K) of the GFLV-GHu RNA1-encoded RNA-dependent RNA polymerase (1EPol) as a modulator of vein-clearing symptom development in N. benthamiana. Mutations to this site abolished (K to G, A, or Q) or attenuated (K to N or P) symptom expression. Noteworthy, residue 802 is necessary but not sufficient for vein clearing, as GFLV-F13 RNA1 carrying K802 remained asymptomatic in N. benthamiana. No correlation was found between symptom expression and RNA1 accumulation, as shown by reverse transcription-quantitative polymerase chain reaction. Additionally, the involvement of RNA silencing of vein clearing was ruled out by virus-induced gene silencing experiments and structure predictions for protein 1EPol suggested that residue 802 is flanked by strongly predicted stable secondary structures, including a conserved motif of unknown function (805LLKT/AHLK/RT/ALR814). Together, these results reveal the protein nature of the GFLV-GHu symptom determinant in N. benthamiana and provide a solid basis for probing and determining the virus-host proteome network for symptoms of vein clearing.

Publisher

Scientific Societies

Subject

Agronomy and Crop Science,General Medicine,Physiology

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