Identification of a Novel Hypovirulence-Inducing Hypovirus From Alternaria alternata

Abstract

Mycoviruses are wide spread throughout almost all groups of fungi but only a small number of mycoviruses can attenuate the growth and virulence of their fungal hosts. Alternaria alternata is an ascomycete fungus that causes leaf spot diseases on various crop plants. In this study, we identified a novel ssRNA mycovirus infecting an A. alternata f. sp. mali strain isolated from an apple orchard in China. Sequence analyses revealed that this virus is related to hypoviruses, in particular to Wuhan insect virus 14, an unclassified hypovirus identified from insect meta-transcriptomics, as well as other hypoviruses belonging to the genus Hypovirus , and therefore this virus is designed as Alternaria alternata hypovirus 1 (AaHV1). The genome of AaHV1 contains a single large open-reading frame encoding a putative polyprotein (∼479 kDa) with a cysteine proteinase-like and replication-associated domains. Curing AaHV1 from the fungal host strain indicated that the virus is responsible for the slow growth and reduced virulence of the host. AaHV1 defective RNA (D-RNA) with internal deletions emerging during fungal subcultures but the presence of D-RNA does not affect AaHV1 accumulation and pathogenicities. Moreover, AaHV1 could replicate and confer hypovirulence in Botryosphaeria dothidea , a fungal pathogen of apple white rot disease. This finding could facilitate better understanding of A. alternata pathogenicity and is relevant for development of biocontrol methods of fungal diseases.

Virome Identification and Characterization of Fusarium sacchari and F. andiyazi: Causative Agents of Pokkah Boeng Disease in Sugarcane

“…Based on BLASTp analysis, the viral-encoded polyprotein had the highest identity (54.1%, coverage 86%, E-value = 0) with the polyprotein encoded by Wuhan insect virus 14 (WIV14), a hypo-like virus identified from insect meta-transcriptomics (Shi et al, 2016). Additionally, this viral protein has identity (29-48%, coverage 45-81%, E-value = 0) to those of Alternaria alternata hypovirus 1 (AaHV1), CHV1, CHV2, and Fusarium graminearum hypovirus 1 (FgHV1) Hillman et al, 1994;Wang et al, 2013;Shi et al, 2016;Li et al, 2019; Supplementary Figure S2). The viral-encoded polyprotein was searched against the conserved domain in NCBI and exhibited three conserved domains, Peptidase_C7 (pfam01830), DUF3525 (pfam12039), and DEAH_box_HrpB (TIGR01970) with low or moderate E-values, which is similar to FgHV1.…”

Molecular and Biological Characterization of the First Hypovirus Identified in Fusarium oxysporum

“…Partial sequence analysis of that dsRNA-2 showed a variable nt identity exclusively with the corresponding nt sequences of FodHV2, but the exact nature of this dsRNA has not been confirmed. The presence of both the complete hypovirus-dsRNA and another, possibly defective-dsRNA has been described for other betahypoviruses, e.g., AaHV1 (Li et al, 2019), BcHV1 (Hao et al, 2018), CHV3/GH2 (Smart et al, 1999), and SsHV1/SZ150 (Xie et al, 2011). In some cases (SsHV1/SZ150), data obtained suggested a contribution of the defective dsRNA to the induction of hypovirulence, but not in others (AaHV1, BcHV1).…”

“…Members of all four currently recognized species in the genus Hypovirus were isolated from C. parasitica (Hillman et al, 1990(Hillman et al, , 1992(Hillman et al, , 1994Enebak et al, 1994;Smart et al, 1999;Linder-Basso et al, 2005;Nuss and Hillman, 2011), but a number of unclassified hypovirus-like viruses have been described infecting other filamentous fungi, e.g., Agaricus bisporus (Deakin et al, 2017), Alternaria alternata (Li et al, 2019), Macrophomina phaseolina (Marzano et al, 2016), Phomopsis longicolla (Koloniuk et al, 2014), Sclerotinia sclerotiorum (Xie et al, 2011;Hu et al, 2014;Khalifa and Pearson, 2014;Marzano et al, 2015), and Valsa ceratosperma (Yaegashi et al, 2012). The only four possible a α β γ: selected viruses from the "Alphahypovirus," the "Betahypovirus," and the "Gammahypovirus" groups, respectively.…”

“…Success in using CHV1 for the biological control of chetnust blight has prompted interest in identifying new members of this family in other phytopathogenic species. Consequently, a number of novel related viruses were isolated from different phytopathogenic fungi, including Alternaria alternata hypovirus 1 (AaHV1; Li et al, 2019), Botrytis cinerea hypovirus 1 (BcHV1; Hao et al, 2018), Entoleuca Hypovirus 1 (EnHV1; Velasco et al, 2018), Phomopsis longicolla hypovirus 1 (PlHV1; Koloniuk et al, 2014), Rosellinia necatrix hypovirus 1 and 2 (RnHV1 and RnHV2; Arjona-Lopez et al, 2018;Velasco et al, 2018), Sclerotinia sclerotiorum hypovirus 1 and 2 (SsHV1 and SsHV2; Xie et al, 2011;Hu et al, 2014), Setosphaeria turcica hypovirus 1 (StHV1; Gilbert et al, 2019), and Valsa ceratosperma hypovirus 1 (VcHV1; Yaegashi et al, 2012). In the genus Fusarium, four putative members of the family Hypoviridae have been identified: Fusarium graminearum hypovirus 1 (FgHV1) from F. graminearum strain HN10 (Wang et al, 2013), Fusarium graminearum hypovirus 2 (FgHV2) from F. graminearum strain SJ16 (Li et al, 2015), Fusarium poae hypovirus 2 (FpHV2) from F. poae strain MAFF 240374 (Osaki et al, 2016), and Fusarium langsethiae hypovirus 1 (FlHV1) from F. langsethiae strain AH32 (Li et al, 2017).…”

A Novel Ourmia-Like Mycovirus Confers Hypovirulence-Associated Traits on Fusarium oxysporum

“…The ssRNA mycoviruses are grouped into seven families: Alphaflexiviridae , Barnaviridae , Botourmiaviridae , Gammaflexiviridae , Hypoviridae , Mymonaviridae , and Narnaviridae ( Amarasinghe et al, 2018 ). There are also unclassified mycoviruses ( Li H. et al, 2019 ).…”