Abstract

Wheat streak mosaic (WSM), a viral disease affecting cereals and grasses, causes substantial losses in crop yields. Wheat streak mosaic virus (WSMV) is the main causal agent of the complex, but mixed infections with Triticum mosaic virus (TriMV) and High plains wheat mosaic emaravirus (HPWMoV) were reported as well. Although resistant varieties are effective for the disease control, a WSMV resistance-breaking isolate and several potential resistance-breaking isolates have been reported, suggesting that viral populations are genetically diverse. Previous phylogenetic studies of WSMV were conducted by focusing only on the virus coat protein (CP) sequence, while there is no such study for either TriMV or HPWMoV. Here, we studied the genetic variation and evolutionary mechanisms of natural populations of WSM-associated viruses mainly in Kansas fields and fields in some other parts of the Great Plains using high-throughput RNA sequencing. In total, 28 historic and field samples were used for total RNA sequencing to obtain full genome sequences of WSM-associated viruses. Field survey results showed WSMV as the predominant virus followed by mixed infections of WSMV + TriMV. Phylogenetic analyses of the full genome sequences demonstrated that WSMV Kansas isolates are widely distributed in sub-clades. In contrast, phylogenetic analyses for TriMV isolates showed no significant diversity. Recombination was identified as the major evolutionary force of WSMV and TriMV variation in KS fields, and positive selection was detected in some encoding genomic regions in the genome of both viruses. Furthermore, the full genome sequence of a second Kansas HPWMoV isolate was reported. Here, we also identified previously unknown WSMV isolates in the Great Plains sharing clades and high nucleotide sequence similarities with Central Europe isolates. The findings of this study will provide more insights into the genetic structure of WSM-associated viruses and, in turn, help in improving strategies for disease management.

Highlights

  • Wheat (Triticum aestivum L.) is one of the leading staple crops in the world

  • Sample screening for Wheat streak mosaic (WSM) viruses using RT-PCR revealed that single infections of Wheat streak mosaic virus (WSMV) dominated Kansas fields at 52% (44 positive out of 84 samples) and 29% (4 positive out of 14 samples) in 2019 and 2020, respectively (Supplementary Table 1)

  • Our study found WSMV as the most prevalent WSM-associated virus in Kansas fields in single infections followed by mixed infections of WSMV + Triticum mosaic virus (TriMV)

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Summary

Introduction

Wheat (Triticum aestivum L.) is one of the leading staple crops in the world. In 2019, the wheat production in Kansas estimated by United States Department of Agriculture’s National Agricultural Statistics Service (USDA NASS) was $1.37 billion (National Agricultural Statistics Service (NASS), 2020). In 2017, a viral disease called wheat streak mosaic (WSM) has caused a total of $76 million in yield loss to Kansas farmers (Hollandbeck et al, 2017). Wheat streak mosaic is a disease complex, which consists of three documented viruses: Wheat streak mosaic virus (WSMV), Triticum mosaic virus (TriMV), and High plains wheat mosaic emaravirus (HPWMoV), which are all transmitted by wheat curl mites (WCM), Aceria tosichella Kiefer (Slykhuis, 1955; Seifers et al, 1997; Seifers et al, 2009). Severe infection may lead to stunted growth (Figure 1; Singh et al, 2018) For this reason, it is difficult to differentiate the causal virus phenotypically from symptoms, and serological or molecular biology techniques such as ELISA and RT-PCR are required to determine which virus or mixed-infection of viruses is present

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