Abstract

Wild plant populations may harbour a myriad of unknown viruses. As the majority of research efforts have targeted economically important plant species, the diversity and prevalence of viruses in the wild has remained largely unknown. However, the recent shift towards metagenomics-based sequencing methodologies, especially those targeting small RNAs, is finally enabling virus discovery from wild hosts. Understanding this diversity of potentially pathogenic microbes in the wild can offer insights into the components of natural biodiversity that promotes long-term coexistence between hosts and parasites in nature, and help predict when and where risks of disease emergence are highest. Here, we used small RNA deep sequencing to identify viruses in Plantago lanceolata populations, and to understand the variation in their prevalence and distribution across the Åland Islands, South-West Finland. By subsequent design of PCR primers, we screened the five most common viruses from two sets of P. lanceolata plants: 164 plants collected from 12 populations irrespective of symptoms, and 90 plants collected from five populations showing conspicuous viral symptoms. In addition to the previously reported species Plantago lanceolata latent virus (PlLV), we found four potentially novel virus species belonging to Caulimovirus, Betapartitivirus, Enamovirus, and Closterovirus genera. Our results show that virus prevalence and diversity varied among the sampled host populations. In six of the virus infected populations only a single virus species was detected, while five of the populations supported between two to five of the studied virus species. In 20% of the infected plants, viruses occurred as coinfections. When the relationship between conspicuous viral symptoms and virus infection was investigated, we found that plants showing symptoms were usually infected (84%), but virus infections were also detected from asymptomatic plants (44%). Jointly, these results reveal a diverse virus community with newly developed tools and protocols that offer exciting opportunities for future studies on the eco-evolutionary dynamics of viruses infecting plants in the wild.

Highlights

  • Plants harbor a wide diversity of microorganisms both inside and outside their tissues, and a fraction of this microbial diversity is known or suspected to be pathogenic (Vandenkoornhuyse et al, 2015)

  • Our results show that the five studied viruses (Plantago lanceolata latent virus, Plantago latent caulimovirus, Plantago betapartitivirus, Plantago enamovirus and Plantago closterovirus) vary in their prevalence across the P. lanceolata populations in the Åland Islands

  • When we compared the abundance of virus specific contigs in the 12 plant populations, we found that in population 1719 both the number of contigs (66 contigs; 45% of all virus specific contigs) and the number of identified viruses was highest, including Plantago lanceolata latent virus (PlLV) (Geminiviridae) and all four putative novel viruses belonging to the Caulimoviridae, Partitiviridae, Luteoviridae and Closteroviridae families

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Summary

Introduction

Plants harbor a wide diversity of microorganisms both inside and outside their tissues, and a fraction of this microbial diversity is known or suspected to be pathogenic (Vandenkoornhuyse et al, 2015). Our understanding of the diversity of potentially pathogenic microbes and their impact on both domesticated plants (Bulgarelli et al, 2015) and model organisms, such as Arabidopsis thaliana (Horton et al, 2014; Müller et al, 2016) has increased dramatically following advances in sequencing technologies. Far less is known about the diversity of potentially pathogenic microbes in natural plant populations. Uncovering pathogen diversity in wild plants is non-trivial as this diversity is expected to impact pathogen epidemiology and evolution as well as virulence suffered by the host (Tollenaere, Susi & Laine, 2016). Understanding the diversity of pathogenic microbes in the wild can offer insights into mechanisms that regulate pathogen populations, and can help predict when and where risks of disease emergence are highest

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