Discovery and Genome Characterization of a Closterovirus from Wheat Plants with Yellowing Leaf Symptoms in Japan

• Published in: Pathogens (Basel) Vol. 12; no. 3; p. 358
• Main Authors: Kondo, Hideki, Sugahara, Hitomi, Fujita, Miki, Hyodo, Kiwamu, Andika, Ida Bagus, Hisano, Hiroshi, Suzuki, Nobuhiro
• Format: Journal Article
• Language: English
• Published: Switzerland MDPI AG 21.02.2023; MDPI
• Subjects: aphid transmission; Barley; Cereal crops; Closterovirus; Crop production; Diseases and pests; Dwarf disease; Genetic aspects; Genomes; Genomics; Growing season; Identification and classification; Insects; Leaves; Next-generation sequencing; Nucleotide sequence; Nucleotides; Open reading frames; Pathogenicity; Pathogens; Phylogeny; Plant viruses; Plants; Plants (botany); Proteins; Rhopalosiphum padi; RNA polymerase; RNA silencing; RNA viruses; RNA-seq; Triticum aestivum; Virus diseases of plants; Virus research; Viruses; Wheat; Winter wheat; Yellow leaf; yellow leaf disease; Yellowing; Japan; aphid transmission; RNA-seq; Japan; yellow leaf disease; wheat; RNA silencing; closterovirus
• ISSN: 2076-0817; 2076-0817
• DOI: 10.3390/pathogens12030358

Many aphid-borne viruses are important pathogens that affect wheat crops worldwide. An aphid-transmitted closterovirus named wheat yellow leaf virus (WYLV) was found to have infected wheat plants in Japan in the 1970s; however, since then, its viral genome sequence and occurrence in the field have not been investigated. We observed yellowing leaves in the 2018/2019 winter wheat-growing season in an experimental field in Japan where WYLV was detected five decades ago. A virome analysis of those yellow leaf samples lead to the discovery of a closterovirus together with a luteovirus (barley yellow dwarf virus PAV variant IIIa). The complete genomic sequence of this closterovirus, named wheat closterovirus 1 isolate WL19a (WhCV1-WL19a), consisted of 15,452 nucleotides harboring nine open reading frames. Additionally, we identified another WhCV1 isolate, WL20, in a wheat sample from the winter wheat-growing season of 2019/2020. A transmission test indicated that WhCV1-WL20 was able to form typical filamentous particles and transmissible by oat bird-cherry aphid ( ). Sequence and phylogenetic analyses showed that WhCV1 was distantly related to members of the genus (family ), suggesting that the virus represents a novel species in the genus. Furthermore, the characterization of WhCV1-WL19a-derived small RNAs using high-throughput sequencing revealed highly abundant 22-nt-class small RNAs potentially derived from the 3'-terminal end of the WhCV1 negative-strand genomic RNA, indicating that this terminal end of the WhCV1 genome is likely particularly targeted for the synthesis of viral small RNAs in wheat plants. Our results provide further knowledge on closterovirus diversity and pathogenicity and suggest that the impact of WhCV1 on wheat production warrants further investigations.