Discovery and analyses of caulimovirid-like sequences in upland cotton (Gossypium hirsutum)

Authors: ABOUGHANEM-SABANADZO, NINA - Mississippi State University; ALLEN, THOMAS - Mississippi State University; Frelichowski, James - Jim; Scheffler, Jodi; SABANADZOVIC, SEAD - Mississippi State University

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/24/2023
Publication Date: 7/28/2023
Citation: Aboughanem-Sabanadzo, N., Allen, T.W., Frelichowski, J.E., Scheffler, J.A., Sabanadzovic, S. 2023. Discovery and analyses of caulimovirid-like sequences in upland cotton (Gossypium hirsutum). Viruses. 15(8). Article 1643. https://doi.org/10.3390/v15081643.
DOI: https://doi.org/10.3390/v15081643

Interpretive Summary: Ancient fragments of DNA from viruses are often found in plants and animals. Some viruses insert their DNA into the host's DNA and then are stably inherited along with the host's DNA. Most of the fragments were inserted thousands to millions of years ago. These fragments are called Endogenous Viral Elements (EVEs). In plants, EVEs over time are duplicated and rearranged and no longer function as a virus. The host plant often repurposes these fragments for other uses including helping prevent infection by functional viruses trying to attack them. We identified a tandem fragment in all the upland cotton we tested and are conducting further tests to see if it may help protect cotton from viruses called Caulimoviridae.

Technical Abstract: Endogenous viral elements (EVEs) are virus-derived sequences which are frequently detected in genomes of numerous plant and animal species. One class of EVEs originate from retroviruses that undergo a reverse transcription step and stably integrate their DNA in the host nuclear genome. These EVEs eventually become fixed in a host species and vertically transmitted throughout subsequent generations. After initial integration, EVEs often undergo amplification and become duplicated or rearranged and are distributed throughout the host genome. They can be repurposed by the host for other uses including protecting the plant from viruses that attempt to infect it. Analyses of Illumina-based high-throughput sequencing data generated during characterization of the cotton leafroll dwarf virus population in Mississippi (2020-2022) consistently yielded contigs varying in size (most frequently from 4 to 7 kb) with identical nucleotide content and sharing similarities with reverse transcriptases (RTases) encoded by existing plant pararetroviruses (family Caulimoviridiae). Initial data prompted an in-depth study involving molecular and bioinformatic approaches to characterize the nature and origins of these caulimovirid-like sequences subsequently identified as EVEs. These EVEs are related to extant members of the family Caulimoviridae, integrated into a genome of upland cotton (Gossypium hirsutum), with the provisional name “endogenous cotton pararetroviral elements” (eCPRVE). A ~15 kbp-long locus on chromosome A04 was identified consisting of head-to-head orientated tandem copies (eCPRVE+ and eCPRVE-). Sequences of the eCPRVE+ comprised near-complete and slightly decayed genome information, including ORFs coding for the viral movement protein (MP), coat protein (CP), and traasactivator/viroplasm protein (TA). Phylogenetic analyses of major viral proteins, suggest that the eCPRVE+ may have been initially derived from a related virus belonging to a putative new genus within the Caulimoviridae family. This EVE was only found in G. hirsutum with the exception of an identical 15 kb locus comprised of two eCPRVE copies detected in the newly recognized species G. ekmanianum, suggesting a relatively recent evolution within the cotton family.