Molecular characterization of a novel cytorhabdovirus with a unique genomic organization infecting yerba mate (Ilex paraguariensis) in Argentina

Abstract

The genome of a novel rhabdovirus was detected in yerba mate (Ilex paraguariensis St. Hil.). The newly identified virus, tentatively named yerba mate virus A (YmVA), has a genome of 14,961 nucleotides.Notably, eight open reading frames were identified in the antigenomic orientation of the negative-sense, single-stranded viral RNA, including two novel accessory genes, in the order 3'-N-P-3-4-M-G-L-8-5'. Sequence identity of the encoded proteins as well as phylogenetic analysis suggest that YmVA is a new member of the genus Cytorhabdovirus, family Rhabdoviridae. YmVA unique genomic organization and phylogenetic relationships indicate that this virus likely represents a distinct evolutionary lineage within the cytorhabdoviruses. Yerba mate (Ilex paraguariensis St. Hil., Aquifoleaceae) is a subtropical tree cultivated in the northeast of Argentina, south of Brazil, and the west of Paraguay. Its leaves and stems are widely utilized in the preparation of an infusion popularly known as "mate." In Argentina, the main producer, the cultivated area has reached 165,327 ha [1]. Although yerba mate is of significant economic, social and traditional importance in the region, studies on plant diseases are still scarce, and only a handful of viruses have been identified in this holly species [2-4] Recently, the complete genome sequence of another cytorhabdovirus was described, associated with chlorotic linear patterns, chlorotic rings, and veins yellowing symptoms in yerba mate, which was named yerba mate chlorosis-associated virus (YmCaV) [3]. The genus Cytorhabdovirus in the family Rhabdoviridae has the largest number of members among the four genera of plant-infecting viruses in the family. Cytorhabdoviruses have a unsegmented, negative-sense, single-stranded RNA genomes with six to ten open reading frames (ORFs) with a canonical genomic organization that includes six proteins in the order 3ʹ-nucleocapsid protein (N) -phosphoprotein (P) -(putative) cell-to-cell movement protein -matrix protein (M) -glycoprotein (G) -polymerase (L) -5ʹ [5]. In this work, we report the molecular characterization of a novel and distinct cytorhabdovirus associated with yerba mate in Argentina, which we tentatively named yerba mate virus A (YmVA).

Illuminating the Plant Rhabdovirus Landscape through Metatranscriptomics Data

“…In the last few years, several novel plant rhabdoviruses, which may be asymptomatic, have been reported in HTS studies [ 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 ]. Thus, it is tempting to speculate that some plant rhabdovirus-like sequences may be hidden in published plant transcriptome databases, generated with diverse objectives beyond virus research, where viral RNA was inadvertently copurified with endogenous plant RNA and sequenced.…”

Development and validation of protocols for virus, viroid and phytoplasma detection to be used for the certification of pome fruit propagation material

“…Out of the 39 apple trees tested, 11 were found positive, 2 in Agia and 9 in Zagora, implying that it is most probably a plant infecting virus. The genome organization was similar to that of rhabdoviruses with some interesting characteristics: the genome seemed to lack the glycoprotein encoding gene, as has been recently described for citrus associated cytorhabdovirus by and encodes for an accessory protein between the L and 5'-trailer, similarly to the genome of yerba mate cytorhabdovirus A (Bejerman et al, 2020). Phylogenetic analysis showed that the new virus grouped within cytorhabdoviruses (Figure 4.13).…”

“…All other predicted proteins had no significant matches with any GenBank deposited sequences. So far, the existence of a gene between L gene and 5'-trailer has only been reported in yerba mate cytorhabdovirus A (Bejerman et al, 2020). Typical for all plant rhabdoviruses, intergenic 'gene junction' conserved regions between ORFs were also identified in ZAGORA_15 sequence (Figure 4.12).…”

Novel tri-segmented rhabdoviruses: A data mining expedition unveils the cryptic diversity of cytorhabdoviruses

“…In the last few years, several novel cytorhabdoviruses which do not induce visible disease symptoms have been reported in HTS studies (Bejerman et al, 2020; Belete et al, 2023; Bolus et al, 2021; Kauffmann et al, 2022; Kopke et al, 2023; Lee et al, 2022; Liu et al, 2021; Medberry et al, 2022; Petrzik et al, 2022; Safarova et al, 2022; Wu et al, 2023). Moreover, many novel cytorhabdoviruses were identified when metatranscriptomic data publicly available at the Transcriptome Shotgun Assembly (TSA) sequence databases was mined (Bejerman et al, 2021).…”

“…Ten betacytorhabdoviruses had two ORFs between the P and M genes, while three others had four ORFs between these genes (Dietzgen et al, 2020). One of these ORFs encodes the putative cell-to-cell movement protein, which is named as P3 in all but the Yerba mate virus A, where this protein is named P4 (Bejerman et al, 2020). The other accessory proteins are named P4, P5 and P6.…”