Transmission of a New Polerovirus Infecting Pepper by the Whitefly Bemisia tabaci

Abstract

Many animal and plant viruses depend on arthropods for their transmission. Virus-vector interactions are highly specific, and only one vector or one of a group of vectors from the same family is able to transmit a given virus. Poleroviruses (Luteoviridae) are phloem-restricted RNA plant viruses that are exclusively transmitted by aphids. Multiple aphid-transmitted polerovirus species commonly infect pepper, causing vein yellowing, leaf rolling, and fruit discoloration. Despite low aphid populations, a recent outbreak with such severe symptoms in many bell pepper farms in Israel led to reinvestigation of the disease and its insect vector. Here we report that this outbreak was caused by a new whitefly (Bemisia tabaci)-transmitted polerovirus, which we named Pepper whitefly-borne vein yellows virus (PeWBVYV). PeWBVYV is highly (Ͼ95%) homologous to Pepper vein yellows virus (PeVYV) from Israel and Greece on its 5= end half, while it is homologous to African eggplant yellows virus (AeYV) on its 3= half. Koch's postulates were proven by constructing a PeWBVYV infectious clone causing the pepper disease, which was in turn transmitted to test pepper plants by B. tabaci but not by aphids. PeWBVYV represents the first report of a whitefly-transmitted polerovirus. IMPORTANCE The high specificity of virus-vector interactions limits the possibility of a given virus changing vectors. Our report describes a new virus from a family of viruses strictly transmitted by aphids which is now transmitted by whiteflies (Bemisia tabaci) and not by aphids. This report presents the first description of polerovirus transmission by whiteflies. Whiteflies are highly resistant to insecticides and disperse over long distances, carrying virus inoculum. Thus, the report of such unusual polerovirus transmission by a supervector has extensive implications for the epidemiology of the virus disease, with ramifications concerning the international trade of agricultural commodities.

Levels of the endosymbiont Rickettsia in the whitefly Bemisia tabaci are influenced by the expression of vitellogenin

“…Be. tabaci is extremely polyphagous and colonizes hundreds of herbaceous plant species (Brown et al, 1995;Secker et al, 1998), inflicting severe damage directly through feeding on host plants and indirectly through honeydew secretion and the transmission of plant viruses (Brown and Czosnek, 2002;Inbar and Gerling, 2008;Ghosh et al, 2019).…”

Whole‐genome single nucleotide polymorphism and mating compatibility studies reveal the presence of distinct species in sub‐Saharan Africa Bemisia tabaci whiteflies

“…Members of the species complex differ greatly in host-plant range (Zang et al, 2006;Xu et al, 2011), inducement of phytotoxic disorders (Sseruwagi et al, 2005;Vyskočilová et al, 2018), resistance to insecticides (Wang et al, 2012;Horowitz & Ishaaya, 2014), invasiveness (Brown et al, 1995;Liu et al, 2007) and specificity of begomovirus transmission (Fiallo-Olivé et al, 2020), which creates challenges in identifying and managing them. The most significant threat posed by B. tabaci is the ability of its members collectively to vector over 300 plant viruses belonging predominantly to the genus Begomovirus, but also including devastating plant viruses from the genera Carlavirus, Crinivirus, Ipomovirus, Polerovirus and Torradovirus (Ng & Falk, 2006;Amari et al, 2008;Navas-Castillo et al, 2011;Zanardo & Carvalho, 2017;Ghosh et al, 2019). In sub-Saharan Africa (SSA), B. tabaci vectors cassava mosaic begomoviruses (CMBs) (Storey & Nichols, 1938) and cassava brown streak ipomoviruses (CBSIs) (Maruthi et al, 2005;Mware et al, 2009).…”

Assessing whitefly diversity to infer about begomovirus dynamics in cassava in Brazil

“…Aleurodicus dispersus and Aleurothrixus trachoides each transmit only one virus from the genera Ipomovirus and Begomovirus, respectively, while Trialeurodes vaporariorum and T. abutilonea transmit a few viruses included in the genera Crinivirus and Torradovirus. On the other hand, the Bemisia tabaci complex comprises one of the most important group of plant virus vectors, transmitting over 430 viruses, the majority included in the genus Begomovirus (12,16) but including also viruses classified in the genera Carlavirus, Crinivirus, Ipomovirus, Polerovrius and Torradovirus (12,(17)(18)(19)(20).…”