Data mining redefines the timeline and geographic spread of cotton leafroll dwarf virus

Authors: OLMEDP-VELARDE, ALEJANDRO - Cornell University; SHAKHZADYAN, HYAK - Cornell University; RETHWISCH, MICHAEL - University Of California Agriculture And Natural Resources (UCANR); WEST-ORTIZ, MICHAEL - Cornell University; WAISEN, PHILLIP - University Of California Agriculture And Natural Resources (UCANR); Heck, Michelle

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/25/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: The United States is the world's leading cotton exporter and ranks third in the global production of cotton, accounting for about 1/3 of global cotton trade. In 2017, cotton leafroll dwarf virus (CLRDV) was reported in Alabama-grown cotton, and in subsequent years, was reported in other cotton growing states. However, genetic analysis of the virus revealed patterns consistent with the idea that CLRDV was not newly introduced. Using data mining, we showed that CLRDV has been in the U.S. for almost 20 years. Datasets from cotton in Louisiana and Mississippi generated in 2015 and 2006, respectively, had CLRDV-derived sequences. These dates are much earlier than the official U.S. detection of CLRDV in 2017. Additionally, CLRDV was found in a cow gut sample from California, suggesting the presence of the virus in a new state. The presence of the virus was corroborated by sampling cotton presenting virus-like symptoms from California and diagnostic assays in the laboratory. The old and new CLRDV sequences clustered in the same group, which strongly suggests CLRDV has been present in the U.S. for much longer than previously thought and is more widespread than initially known. Using datasets that were generated before official reports of CLRDV in both China and India also revealed the presence of CLRDV. This information is vital to understanding how the virus spreads and for developing strategies to control it. Importantly, this new information suggests that CLRDV was possibly not causing obvious symptoms before 2017 and suggests that future research on biotic or abiotic factors is required to understand CLRDV symptomatology and epidemiology.

Technical Abstract: Cotton leafroll dwarf virus (CLRDV), a threat to the cotton industry, was first reported in the United States (US) as an emergent pathogen in 2017. Phylogenetic analysis supports the hypothesis that US CLRDV strains are genetically distinct from strains in South America and elsewhere, which is not consistent with the hypothesis that the virus is newly introduced into the country. Therefore, using database mining, we evaluated the timeline and geographic distribution of CLRDV in the country. We uncovered evidence that shows that CLRDV had been in the US for over a decade before its official first report. CLRDV sequences were detected in datasets derived from Mississippi in 2006, Louisiana in 2015, and California in 2018. Additionally, through field surveys of upland cotton in 2023, we confirmed that CLRDV is present in California, which had no prior reports of the virus. Viral sequences from these old and new datasets exhibited high nucleotide identities (>98%) with recently characterized US isolates, and phylogenetic analyses with their homologs placed these sequences within a US-specific clade, further supporting the earlier presence of CLRDV in the country. Moreover, potential new hosts, including another fiber crop, flax, were determined through data mining. Retrospective analysis suggests CLRDV presence in the US since at least 2006 (Mississippi). These findings necessitate a reevaluation of spread patterns, inoculum sources, symptomology variations, and control strategies. Our findings challenge the current understanding of the arrival and spread of CLRDV in the US, highlight the power of data mining for virus discovery, and underscore the need for further investigation into CLRDV's impact on US cotton.