Rice Dwarf Viruses with Dysfunctional Genomes Generated in Plants Are Filtered Out in Vector Insects: Implications for the Origin of the Virus

Abstract

Rice dwarf virus (RDV), with 12 double-stranded RNA (dsRNA) genome segments (S1 to S12), replicates in and is transmitted by vector insects. The RDV-plant host-vector insect system allows us to examine the evolution, adaptation, and population genetics of a plant virus. We compared the effects of long-term maintenance of RDV on population structures in its two hosts. The maintenance of RDV in rice plants for several years resulted in gradual accumulation of nonsense mutations in S2 and S10, absence of expression of the encoded proteins, and complete loss of transmissibility. RDV maintained in cultured insect cells for 6 years retained an intact protein-encoding genome. Thus, the structural P2 protein encoded by S2 and the nonstructural Pns10 protein encoded by S10 of RDV are subject to different selective pressures in the two hosts, and mutations accumulating in the host plant are detrimental in vector insects. However, one round of propagation in insect cells or individuals purged the populations of RDV that had accumulated deleterious mutations in host plants, with exclusive survival of fully competent RDV. Our results suggest that during the course of evolution, an ancestral form of RDV, of insect virus origin, might have acquired the ability to replicate in a host plant, given its reproducible mutations in the host plant that abolish vector transmissibility and viability in nature.Most plant viruses are transmitted by insects in various ways that are classified into nonpersistent, semipersistent, and persistent transmissions, depending primarily on the times of acquisition, latency, and retention (5). A variety of interactions among plants, viruses, and insects are involved in viral propagation, and the prerequisite intimate relationships impose selective pressure, shape viral populations, and influence viral evolution. Plant viruses maintained exclusively in host plants without transmission by insect vectors accumulate mutations that are detrimental to vector transmissibility, regardless of the mode of transmission, and emerge as transmission-defective (TD) strains (3). Representative examples of this phenomenon are provided by potyviruses (nonpersistent) (18), cucumovirus (nonpersistent) (10), and tospoviruses (propagative) (24), in which mutations occur mostly in genes for structural proteins and/or transmission helper components (nonstructural proteins) assumed to interact with insect partners. Plant viruses transmitted in a propagative manner, a persistent mode of transmission that involves replication in vectors, allow us to examine the genetic effects of the maintenance of such viruses in either host.Rice dwarf virus (RDV) is a member of the family Reoviridae, one of the largest virus families, with a wide range of hosts from fungi to plants, insects, nonhuman vertebrates, and humans (1). RDV has a double-stranded RNA (dsRNA) genome consisting of 12 segments (S1 to S12). It induces dwarf symptoms with leaf specks in monocotyledonous plant hosts and can replicate in vector insects, such as leafhoppers....

Rice Reoviruses in Insect Vectors

“…The maintenance of RDV in rice plants for several years without feeding by insects results in gradual accumulation of nonsense mutations in the P2 or Pns10 genes and the complete loss of transmissibility of the mutant virus by insect vectors (50,89). When RDV is maintained in the intact insect for six years via vertical transmission, it retains an intact protein-encoding genome (41,89).…”

“…The implication for the origin of RDV may be deduced from the RDV-leafhopper-rice system (89). When RDV is maintained only in the host plants, defective interfering (DI) RNAs with nonsense mutations in the P2 and Pns10 genes are gradually fixed, and wild RNAs with the fulllength P2 and Pns10 genes gradually diminish.…”

Sequenciamento e análise da variabilidade genética de vírus transmitidos por ácaros do gênero <i>Brevipalpus </i>no Brasil

“…Esses VTB afetam culturas, como café e maracujá, além de mais de 50 espécies de plantas ornamentais BOARI et al, 2011;RAMALHO et al, 2014;ROY et al, 2015a).…”

“…O cafeeiro é também uma cultura relevante para o agronegócio brasileiro (BOARI et al, 2011), e ao nível mundial é considerado o quinto produto que gera mais riqueza (RAMALHO et al, 2014). O Brasil é o maior produtor e exportador mundial de café e segundo maior consumidor do produto.…”

“…A produtividade e qualidade do café são influenciadas por diversos fatores, dentre eles a ocorrência de doenças (BOARI, 2011) que podem ser causadas por fungos, bactérias, nematoides e vírus. A principal doença causada por vírus que afeta o cafeeiro é conhecida como a mancha anular do cafeeiro (FIGUEIRA et al, 1995) a qual está atualmente distribuída na maioria dos estados brasileiros e na Costa Rica (KITAJIMA et al, 2011a;ALMEIDA et al, 2012;RAMALHO et al, 2014;.…”