A Victorivirus and Two Novel Mitoviruses Co-Infected the Plant Pathogen Nigrospora oryzae

Abstract

Three dsRNAs, in sizes of approximately 2.5–5 kbp, were detected in the plant pathogenic fungus Nigrospora oryzae strain CS-7.5-4. Genomic analysis showed that the 5.0 kb dsRNA was a victorivirus named as Nigrospora oryzae victorivirus 2 (NoRV2). The genome of NoRV2 was 5166 bp in length containing two overlapping open reading frames (ORFs), ORF1 and ORF2. ORF1 was deduced to encode a coat protein (CP) showing homology to the CPs of viruses belonging to the Totiviridae family. The stop codon of ORF1 and the start codon of ORF2 were overlapped by the tetranucleotide sequence AUGA. ORF2 was predicted to encode an RNA-dependent RNA polymerase (RdRp), which was highly similar to the RdRps of victoriviruses. Virus-like particle examination demonstrated that the genome of NoRV2 was solely encapsidated by viral particles with a diameter of approximately 35 nm. The other two dsRNAs that were less than 3.0 kb were predicted to be the genomes of two mitoviruses, named as Nigrospora oryzae mitovirus 1 (NoMV1) and Nigrospora oryzae mitovirus 2 (NoMV2). Both NoMV1 and NoMV2 were A-U rich and with lengths of 2865 and 2507 bp, respectively. Mitochondrial codon usage inferred that each of the two mitoviruses contains a major large ORF encoding a mitoviral RdRp. Horizontal transfer experiments showed that the NoMV1 and NoMV2 could be cotransmitted horizontally via hyphal contact to other virus-free N. oryzae strains and causes phenotypic change to the recipient, such as an increase in growth rate. This is the first report of mitoviruses in N. oryzae.

Characterization of a Novel Mitovirus Infecting Melanconiella theae Isolated From Tea Plants

“…Since mitoviruses essentially replicate within mitochondria of their hosts ( Polashock and Hillman, 1994 ; Cole et al, 2000 ; Osaki et al, 2005 ; Nibert, 2017 ; Fonseca et al, 2021 ), MtMV1 genome shares the most features of mitochondrial codons described before, e.g., the MtMV1 genome contains ten UGA codons, which encode Trp rather than function as a stop codon ( Nibert, 2017 ; Vong et al, 2019 ), while only two UGG, and has rich of A-U content (62.37%) like other members (59.55 to 73.25%). Moreover, the initiation codon of MtMV1 ORF has a preference to be either A or U with a frequency of 68.3% in the third nucleotide position, similar to those of other members ( Liu et al, 2019 ; Torres-Trenas and Pérez-Artés, 2020 ; Wang et al, 2021 ) and has a UAG stop codon, similar to the observation in other members with either UAA or UAG ( Nibert, 2017 ). Additionally, the 5′- and 3′-terminus sequences of MtMV1 could be folded into stem-loop structures, and their reverse complementary regions allow to form a stable panhandle structure, which is also observed in other members ( Hong et al, 1999 ; Khalifa and Pearson, 2013 ; Wang et al, 2021 ).…”

“…Mitoviruses (family Mitoviridae ) represent the simplest group of all RNA viruses ( Hillman and Cai, 2013 ), with a unique genome of + ssRNA which ranges in size between 2.0 and 4.5 kb, encompassing a single long open reading frame (ORF) which encodes a putative RNA-dependent RNA polymerase (RdRp) with six conserved amino acid motifs (I–IV) ( Osaki et al, 2015 ; Ran et al, 2016 ; Chen et al, 2017 ; Wang et al, 2019 ; Kocanová et al, 2020 ; Liu et al, 2021 ). Their Genomes are AU rich, especially in the third position of codons ( Hong et al, 1998 ; Xie and Ghabrial, 2012 ; Liu et al, 2019 ; Torres-Trenas and Pérez-Artés, 2020 ; Wang et al, 2021 ). Mitoviral genomes are characterized by multiple UGA codons encode tryptophan (Trp) instead of stop translation ( Nibert, 2017 ; Nibert et al, 2019 ); however, the termination codon is usually UAA and sometimes UAG ( Nibert, 2017 ).…”

Characterization of the Mycovirome of the Phytopathogenic Fungus, Neofusicoccum parvum

“…Nevertheless, these results indicate a very high Narnaviridae and Mitoviridae diversity associated with N. parvum. Although most of the mitoviruses and narnaviruses are associated with symptomless infections [32], some exceptions have been described, such as two mitoviruses recently characterized from Nigrospora oryzae that can be co-transmitted horizontally and can modulate positively the growth rate of the recipient N. oryzae isolate [43]. Hypovirulence related to a mitovirus has also been documented in the phytopathogenic fungus Sclerotinia sclerotiorum [44].…”

Molecular characterization of a novel victorivirus infecting Corynespora cassiicola

“…In the Totiviridae family, Totivirus and Victorivirus exclusively infect with fungus [10]. The viruses of the genus Victorivirus infect various phytopathogenic fungi, including Ustilaginoidea virens [11], Nigrospora oryzae [12], Fusarium asiaticum [13], Aspergillus foetidus [14], Macrophomina phaseolina [15] and Rosellinia necatrix [16]. The coding strands of victoriviruses usually have two large open reading frames (ORFs) with the 5′-proximal ORF encoding the coat protein (CP) and the 3′-proximal ORF encoding the RNA-dependent RNA polymerase (RdRp) [17].…”