Ecological and Genetic Determinants of Pepino Mosaic Virus Emergence

Abstract

Virus emergence is a complex phenomenon, which generally involves spread to a new host from a wild host, followed by adaptation to the new host. Although viruses account for the largest fraction of emerging crop pathogens, knowledge about their emergence is incomplete. We address here the question of whether Pepino mosaic virus (PepMV) emergence as a major tomato pathogen worldwide could have involved spread from wild to cultivated plant species and host adaptation. For this, we surveyed natural populations of wild tomatoes in southern Peru for PepMV infection. PepMV incidence, genetic variation, population structure, and accumulation in various hosts were analyzed. PepMV incidence in wild tomatoes was high, and a strain not yet reported in domestic tomato was characterized. This strain had a wide host range within the Solanaceae, multiplying efficiently in most assayed Solanum species and being adapted to wild tomato hosts. Conversely, PepMV isolates from tomato crops showed evidence of adaptation to domestic tomato, possibly traded against adaptation to wild tomatoes. Phylogenetic reconstructions indicated that the most probable ancestral sequence came from a wild Solanum species. A high incidence of PepMV in wild tomato relatives would favor virus spread to crops and its efficient multiplication in different Solanum species, including tomato, allowing its establishment as an epidemic pathogen. Later, adaptation to tomato, traded off against adaptation to other Solanum species, would isolate tomato populations from those in other hosts. IMPORTANCE Virus emergence is a complex phenomenon involving multiple ecological and genetic factors and is considered to involve three phases: virus encounter with the new host, virus adaptation to the new host, and changes in the epidemiological dynamics.We analyze here if this was the case in the recent emergence of Pepino mosaic virus (PepMV) in tomato crops worldwide. We characterized a new strain of PepMV infecting wild tomato populations in Peru. Comparison of this strain with PepMV isolates from tomato crops, plus phylogenetic reconstructions, supports a scenario in which PepMV would have spread to crops from wild tomato relatives, followed by adaptation to the new host and eventually leading to population isolation. Our data, which derive from the analysis of field isolates rather than from experimental evolution approaches, significantly contribute to understanding of plant virus emergence, which is necessary for its anticipation and prevention.

Genetic variation and evolutionary analysis of Pepino mosaic virus in Sicily: insights into the dispersion and epidemiology

“…The first PepMV isolates in Europe shared about 99% nucleotide identity and they were considered to be the European strain (EU) (Hanssen & Thomma, ). After 2005, isolates of the EU strain were replaced by isolates of the CH2 strain (with nucleotide identities about 80% between isolates of different strains) (Pagán et al ., ; Gómez et al ., ; Moreno‐Pérez et al ., ). The discovery that the Sicilian PepMV isolates in this study were related to the CH2 strain was expected from the relatively recent emergence of PepMV in Sicily.…”

“…Pepino mosaic virus is currently classified into six strains based on molecular and biological characteristics: European strain (EU), North American strain (US1/CH1), Chilean strain (CH2), the recombinant strain (US2), the original Peruvian strain (LP), and the new Peruvian strain (PES) (Hanssen & Thomma, ; Moreno‐Pérez et al ., ).…”

“…In Europe the EU strain spread first (Cotillon et al ., ; Salomone & Roggero, ; Pagán et al ., ), but later the CH2 strain became predominant (Gómez et al ., ; Moreno‐Pérez et al ., ). The first PepMV outbreak in Sicily occurred in a single greenhouse in 2005, and was quickly eradicated (Davino et al ., ).…”

Host range and symptomatology of Pepino mosaic virus strains occurring in Europe

“…However, in general they show significantly less clear symptoms in these plants (except tobacco). This could point to a specific adaptation of these strains to solanaceous species other than their alleged original wild S. lycopersicon hosts (Moreno-Pérez et al 2014). It remains to be tested if this adaptation indeed went to the expense of their ability to infect wild S. lycopersicon hosts.…”

“…In a recent paper Moreno-Pérez et al (2014) concluded from a study on PepMV in wild Solanum species in Peru that host adaptation of PepMV isolates likely played in role in the infections in domesticated tomatoes as observed since 1999. They conclude that the most probable ancestral sequence of PepMV came from a wild Solanum species and that a high incidence of PepMV in wild tomato relatives would favour virus spread to crops and its efficient multiplication in different Solanum species, including tomato, allowing its establishment as an epidemic pathogen.…”