Thrips Vectors and Tospoviruses: On the Edge of Adaptation
Ullman D
Department of Entomology, University of California, One Shields Avenue, Davis. CA 05616-8584 USA.
Correspondence: deullman@ucdavis.edu
The coevolution of insect vectors and the viruses they transmit represents one of the most fascinating systems in which evolution and its consequences can be studied in observable time spans (reviewed in Whitfield AE et al. 2005. Annual Review of Phytopathology 43: 17.1每17.31). Evolutionary processes in viruses are at the root of their of their pathogenic potential and certainly this is true of viruses in the genus Tospovirus. Although less is known about the thrips genome, their diversity and rapid adaptation to environmental challenges (e.g. pesticide resistance) suggests evolutionary processes also fuel their success and emergence as pests. Testimony to the likely importance of thrips-tospovirus coevolution can be found in the emergence of at least 13 new tospovirus species and at least three new thrips vector species over the past 15 years. Although tospoviruses can be mechanically transmitted under experimental conditions, tospovirus dispersal and survival in nature depends on passage to plants by thrips vectors. The dispersal and survival of TSWV depends upon: a) coexistence of virus and vector populations under conditions of genetic and physiological compatibility; and, b) environmental and plant-host interactions with the virus and the insect allowing every phase of the infection cycle. Thus, coevolution between thrips and tospoviruses must greatly influence the observed variability between virus isolates, epidemics, and even the emergence of new tospoviruses. Tremendous genetic variability in tospovirus populations is provided by the high error rate inherent in RNA replication by the viral RdRp and the reassortment of genomic segments between different virus isolates in planta (Ullman D et al. 2005. Proceedings of the National Academy of Science USA 102:4931每4932). Sin et al. (2005, Proceedings of the National Academy of Science USA 102:5168每5173) showed that the genetic determinants of insect transmission of TSWV lie on the viral M RNA. In mixed infections of a thrips transmissible and a thrips non-transmissible isolate reassortment occurred and a specific mutation on the M RNA was shown to eliminate insect transmissibility. Little is known about the thrips genome, but all of the vector species are characterized by striking morphological diversity, which suggests genetically variable populations. Tospovirus and thrips vector populations certainly meet the basic requirements for rapid coevolution. It seems likely coevolution between thrips and tospoviruses, the potential for TSWV reassortment, and the role of M RNA in determining transmissibility all play critical roles in the emergence of new vector-virus relationships.
The curious incident of the thrips and the Tospovirus
Ullman D
Department of Entomology, University of California, One Shields Avenue, Davis, CA 95616-8584 USA.
Correspondence: deullman@ucdavis.edu
Insect vectors play a key role in dissemination of viruses causing important diseases of humans, animal and plants. Specific understanding of insect-virus interactions leading to successful transmission is a central problem in vector biology and critical to developing novel control strategies (Ullman DE, et al. 2005. Proceedings of the National Academy of Science USA 102: 4931每4932). Tomato spotted wilt virus (TSWV) is the type member of the genus Tospovirus in which at least 15 virus species are proposed. The Tospoviruses are transmitted between plants by at least 10 species of thrips (Thripidae, Thysanoptera) and are the only plant-infecting members in the family Bunyaviridae. The cellular and molecular determinants underlying the thrips 每 tospovirus relationship and vector competence are biological mysteries fueling intense research by entomologists and virologists worldwide. Certainly, the complex nature of the interplay between thrips, tospoviruses and their shared plant hosts make them ideal model systems for elucidating processes of virus infection in disparate hosts that can be extended to solutions for tospovirus epidemics in crops and to controlling viruses of importance to human health. The discoveries that have advanced our understanding of the interface between thrips and the tospoviruses they transmit have been driven by an understanding of thrips internal anatomy and physiology and the genome strategies and biology of the tospoviruses. The finding that tospoviruses multiplied in their thrips vectors opened rich and exciting avenues of exploration, including understanding biological and molecular interactions underlying TSWV pathogenesis in plant and insect hosts and the role these processes play in virus evolution. Discoveries during the last decade show that insect inoculation of tospoviruses into a plant host cannot occur without viral passage across at least three insect organs (the midgut, visceral muscle cells and salivary glands) that include six membrane barriers (Whitfield AE et al. 2005. Annual Review of Phytopathology 43: 17.1每17.31). Attention on thrips internal anatomy, development and thrips-tospovirus interactions have revealed much about the pathway of the virus in the insect, the membrane barriers to virus passage and the importance of ontogeny to virus acquisition and vector competence. The hypothesis that tospovirus glycoproteins are essential determinants of thrips acquisition has been advanced significantly through two important breakthroughs: a) Whitfield et al. 2005 (Virus Research 110:183每86) developed a system to express the GPs, study their structure and function and experimentally manipulate their interactions with the insects; and, b) Sin et al. 2005. (Proceedings of the National Academy of Science USA 102:5168每5173) refined use of viral reassortants to study the impact of specific virus mutations on thrips acquisition. Stumpf CF and Kennedy GG. 2005. (Entomologia Experimentalis et Applicata 114:215每25) used this same system of reassortants to advance our knowledge of the interactions between virus genetic diversity and ecological and physiological factors impacting thrips transmission of tospoviruses. Clearly, we have entered an era in which understanding of TSWV-thrips vector interactions can advance as never before. Translation of these fundamental advances into creative new control strategies will be a significant, but exciting challenge in the years to come.
