What a tangled web we weave: how agriculture, a polyphagous insect vector, and rampant recombination drove the emergence, evolution, and economic importance of the geminivirus beet curly top virus in western North America

ABSTRACT Curly top disease (CTD) of sugar beet is characterized by leaf curling and stunted growth. Historic CTD emerged independently in western North America (~1900), South America (~1925), and the Middle East (~1955), following intensive cultivation of this Old World crop. In these regions, CTD is caused by genetically distinct monopartite geminiviruses transmitted by different leafhopper species. In North America, CTD is caused by 11 strains of beet curly top virus (BCTV) and transmitted by the beet leafhopper (BLH, Circulifer tenellus ). Here, the emergence and evolution of BCTV and the role of agriculture were investigated using 133 genome sequences of isolates collected from multiple crops and locations over nearly a century, including 32 recent sequences from New World (NW) crops in California. New strains were not identified, and all isolates are recombinant and have four conserved breakpoints. Recombination-aware evolutionary analyses estimated BCTV emerged ~750 years ago, likely from a progenitor infecting uncultivated NW plants. Diversification was associated with the domestication of NW crops, especially pepper; the introduction of sugar beet; and the emergence of mild- and severe-type sugar beet strains. Overgrazing of grasses in foothills allowed proliferation of weed reservoirs of BCTV and BLH. Isolates recently collected from NW crops and weeds were mostly mild-type strains, revealing a strain shift. The C4 effector protein of mild-type strains is nearly completely disordered (99%) compared with 44% for severe-type strains, suggesting a role in adaptive evolution. Thus, the evolution of BCTV and CTD biology were driven by agricultural practices, genetic flexibility of BCTV, and the polyphagous BLH vector. IMPORTANCE This study revealed how the emergence and evolution of beet curly top virus (BCTV) and curly top disease in the western United States beginning ~ 1900 was facilitated by agriculture. Results of historic and molecular genetic studies showed BCTV emerged and diversified during the domestication of New World (NW) crops and subsequently after the introduction and intensification of Old World sugar beet. Invasive dicot weeds colonizing overgrazed foothill areas provided reservoirs for BCTV and the beet leafhopper vector. The long evolutionary history of BCTV, mediated by recombination and genetic drift, resulted in strains adapted to sugar beet (severe-type) and NW crops (mild-type). Following reduced sugar beet cultivation in California, mild-type strains underwent population expansion and became predominant in NW crops, facilitated by a highly disordered C4 effector protein. Thus, the genetic flexibility of BCTV, the polyphagous vector, and changing agricultural practices drove the emergence and persistence of this economically important plant disease.