Sixty Years from the First Disease Description, a Novel Badnavirus Associated with Chestnut Mosaic Disease

Abstract

Although the chestnut mosaic disease (ChMD) was described several decades ago, its etiology is still not elucidated. Here, using classical approaches in combination with high throughput sequencing (HTS) techniques, we identify a novel Badnavirus that is a strong etiological candidate for ChMD. Two disease sources from Italy and France were submitted to HTS-based viral indexing. Total RNAs were extracted, ribodepleted and sequenced on an Illumina NextSeq500 (2x150 or 2x 75 nt). In each source, we identified a single contig of about 7.2 kilobases that corresponds to a complete circular viral genome and shares homologies with various badnaviruses. The genomes of the two isolates have an average nucleotide identity of 90.5% with a typical badnaviral genome organization comprising three open reading frames. Phylogenetic analyses and sequence comparisons show that this virus is a novel species for which we propose the name Chestnut mosaic virus (ChMV). Using a newly developed molecular detection test, we systematically detected the virus in symptomatic graft-inoculated indicator plants (chestnut and American oak), as well in chestnut trees presenting typical ChMD symptoms in the field (100% and 87% in France and Italy surveys, respectively). Datamining of publicly available chestnut SRA transcriptomic data allowed the reconstruction of two additional complete ChMV genomes from two Castanea mollissima sources from the USA, as well as ChMV detection in C. dentata from the USA. Preliminary epidemiological studies, performed in France and in Central Eastern Italy, showed that ChMV has a high incidence in some commercial orchards, with a low within-orchard genetic diversity.

Emerging and Re-Emerging Diseases Caused by Badnaviruses

“…Badnaviruses are also reported to infect several ornamentals, medicinal herbs, fruits, trees, and weeds [ 154 , 155 , 156 , 157 , 158 , 159 , 160 , 161 , 162 , 163 , 164 , 165 , 166 , 167 , 168 , 169 , 170 , 171 , 172 , 173 , 174 , 175 , 176 , 177 , 178 , 179 , 180 , 181 , 182 , 183 , 184 , 185 , 186 , 187 , 188 , 189 ]. Birch leaf roll-associated virus, pagoda yellow mosaic-associated virus, and mulberry badnavirus 1 are known to infect different tree crops ( Table 1 ) [ 156 , 157 , 158 ].…”

Towards the Forest Virome: High-Throughput Sequencing Drastically Expands Our Understanding on Virosphere in Temperate Forest Ecosystems

“…Among these, three virus genera are overwhelmingly represented. These are the genus Emaravirus with four species to date (aspen mosaic-associated virus [ 42 ], common oak ringspot-associated virus [ 56 , 57 ], maple mottle-associated virus [ 74 ] and European mountain ash ringspot-associated virus [ 16 ]), the genus Badnavirus with two species (birch leafroll-associated virus [ 15 ] and chestnut mosaic virus [ 55 ]) and the genus Carlavirus with eight species (birch carlavirus [ 14 ], blueberry scorch virus [ 43 , 44 ], elderberry carlaviruses A, B, C, D, E [ 59 , 60 ] and elm carlavirus [ 61 , 62 , 63 ]). All the novel emara- and badnaviruses are found to be associated with the corresponding symptoms and are, consequently, plant pathogenic, while the role of carlaviruses is not yet clarified.…”

“…In 1987, it was reported in France [ 193 ], involving necrotic lesions in the bark and wood that turn into cankers, chlorotic lesions and yellow stripes on leaf veins and partial limb atrophy, thus heavily affecting the production [ 194 ]. By using RNA-Seq analysis, two independent isolates of the same novel virus were identified [ 55 ]. The novel chestnut mosaic virus belongs to the genus Badnavirus , family Caulimoviridae ; it is unambiguously proven to be episomal and is strongly suggested to play causal role in the disease development.…”

Towards the Forest Virome: Next-Generation-Sequencing Drastically Expands our Understanding on Virosphere in Temperate Forest Ecosystems

“…Among these, three virus genera are overwhelmingly represented. These are the genus Emaravirus with up to now four species (aspen mosaic-associated virus [26]; common oak ringspot-associated virus [27,28]; maple mottle-associated virus [29]; European mountain ash ringspot-associated virus [9]), the genus Badnavirus with two species (birch leafroll-associated virus [15]; chestnut mosaic virus [30]) and the genus Carlavirus with eight species (birch carlavirus [14]; blueberry scorch virus [31]; elderberry carlaviruses A, B, C, D, E [32][33]; elm carlavirus [34]). All the novel emara-and badnaviruses are found to be associated with the corresponding symptoms and are, consequently, plant pathogenic, while the role of the carlaviruses is not yet clarified.…”

“…The disease was described several decades ago in Italy [78] associated with viral symptoms like mosaic, shoots with asymmetric leaf blade deformation.Later, it was reported in France in 1987 [79] involving necrotic lesions in the bark and wood that turns into cankers, chlorotic lesions and yellow stripes on leaf veins and partial limb atrophy and, consequently, heavily affecting the production [80]. By using RNA-Seq analysis, two independent isolates of the same novel virus were identified [30]. The novel chestnut mosaic virus belongs to the genus Badnavirus, family Caulimoviridae, it is unambiguously proven to be episomal and is strongly suggested to play causal role in the disease development.…”