Co-Infection by Two Criniviruses Alters Accumulation of Each Virus in a Host-Specific Manner and Influences Efficiency of Virus Transmission

Abstract

Tomato chlorosis virus (ToCV), and Tomato infectious chlorosis virus (TICV), family Closteroviridae, genus Crinivirus, cause interveinal chlorosis, leaf brittleness, and limited necrotic flecking or bronzing on tomato leaves. Both viruses cause a decline in plant vigor and reduce fruit yield, and are emerging as serious production problems for field and greenhouse tomato growers in many parts of the world. The viruses have been found together in tomato, indicating that infection by one Crinivirus sp. does not prevent infection by a second. Transmission efficiency and virus persistence in the vector varies significantly among the four different whitefly vectors of ToCV; Bemisia tabaci biotypes A and B, Trialeurodes abutilonea, and T. vaporariorum. Only T. vaporariorum can transmit TICV. In order to elucidate the effects of co-infection on Crinivirus sp. accumulation and transmission efficiency, we established Physalis wrightii and Nicotiana benthamiana source plants, containing either TICV or ToCV alone or both viruses together. Vectors were allowed to feed separately on all virus sources, as well as virus-free plants, then were transferred to young plants of both host species. Plants were tested by quantitative reverse-transcription polymerase chain reaction, and results indicated host-specific differences in accumulation by TICV and ToCV and alteration of accumulation patterns during co-infection compared with single infection. In N. benthamiana, TICV titers increased during co-infection compared with levels in single infection, while ToCV titers decreased. However, in P. wrightii, titers of both TICV and ToCV decreased during mixed infection compared with single infection, although to different degrees. Vector transmission efficiency of both viruses corresponded with virus concentration in the host in both single and mixed infections. This illustrates that Crinivirus epidemiology is impacted not only by vector transmission specificity and incidence of hosts but also by interactions between viruses and efficiency of accumulation in host plants.

Application of game theory to the interaction between plant viruses during mixed infections

“…However, just focusing on plant viruses, the same interaction described here has been observed for several other pairs of viruses (Hii et al, 2002;Kokkinos & Clark, 2006;Zeng et al, 2007;Wintermantel et al, 2008). In other interactions, however, both viruses gain an advantage (Scheets, 1998;Hii et al, 2002), both viruses pay a cost (Wintermantel et al, 2008), one of them gains whereas the other is not apparently affected (Wang et al, 2002(Wang et al, , 2004Wege & Siegmund, 2007) or one pays a cost whilst the other remains unaffected (Pohl & Wege, 2007).…”

“…Detection techniques used in most previous reports on mixed infections have been aimed at comparing the accumulation of each competing virus in singly versus coinfected plants, but to our knowledge, relative accumulation among competing viruses has been estimated only in a few instances (Scheets, 1998;Kokkinos & Clark, 2006;Zeng et al, 2007;Wintermantel et al, 2008). To determine an estimate of the relative fitness of our competing viruses, TuMV was titrated by RT-qPCR and CaMV by qPCR using an absolute quantification method.…”

“…Mixed infections can also modify viral traits such as host range (Guerini & Murphy, 1999;Hacker & Fowler, 2000;García-Cano et al, 2006), transmission rate (Rochow, 1970;Kuhn & Dawson, 1973;Wintermantel et al, 2008), cellular tropism (Wege & Siegmund, 2007) and titre. Most studies have focused on synergistic diseases caused by two single-stranded (ss) DNA or ssRNA viruses, particularly by a member of the genus Potyvirus and another ssRNA virus.…”

Evolution and Emergence of Plant Viruses

“…In an individual host, coinfection may have variable consequences, from the development of milder symptoms to their exacerbation (Hammond et al, 1999). Mixed infections also affect traits such as the host range (García-Cano et al, 2006;Guerini & Murphy, 1999;Hacker & Fowler, 2000), the rate of transmission (Wintermantel et al, 2008), cellular tropism (Moreno et al, 1997;Sánchez-Navarro et al, 2006), or viral accumulation (Martín & Elena, 2009). …”

The virulence–transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies

“…Even if no general trend arises from results concerning viral mutant genotypes, such studies demonstrate the existence of variation in the relationships between viral accumulation and virulence or symptom severity. Unfortunately, studies that reported the phenotype of natural isolates often measured only virulence (Yahara & Oyama 1993;Lapidot et al 1997;Maskell et al 1999;Funayama-Noguchi 2001;Malmstrom et al 2005Malmstrom et al , 2006 or viral accumulation (Fargette et al 1987;Llamas-Llamas et al 1998;Thurston et al 2001;Untiveros et al 2007;Wintermantel et al 2008) of one viral isolate in one or several host genotypes in different environments. To our knowledge, only a handful of studies have measured both phenotypes concomitantly for several viral natural isolates after individual inoculation of one host genotype.…”