The proposed new species, cacao red vein virus, and three previously recognized badnavirus species are associated with cacao swollen shoot disease

Abstract

Background Cacao swollen shoot virus (CSSV), Cacao swollen shoot CD virus (CSSCDV), and Cacao swollen shoot Togo A virus (CSSTAV) cause cacao swollen shoot disease (CSSD) in West Africa. During 2000–2003, leaf and shoot-swelling symptoms and rapid tree death were observed in cacao in Cote d’Ivoire and Ghana. Molecular tests showed positive infection in only ~50–60% of symptomatic trees, suggesting the possible emergence of an unknown badnavirus.MethodsThe DNA virome was determined from symptomatic cacao samples using Illumina-Hi Seq, and sequence accuracy was verified by Sanger sequencing. The resultant 14, and seven previously known, full-length badnaviral genomic and RT-RNase H sequences were analyzed by pairwise distance analysis to resolve species relationships, and by Maximum likelihood (ML) to reconstruct phylogenetic relationships. The viral coding and non-coding sequences, genome organization, and predicted conserved protein domains (CPDs) were identified and characterized at the species level.ResultsThe 21 CSSD-badnaviral genomes and RT-RNase H sequences shared 70–100% and 72–100% identity, respectively. The RT-RNase H analysis predicted four species, based on an ≥80% species cutoff. The ML genome sequence tree resolved three well-supported clades, with ≥70% bootstrap, whereas, the RT-RNase H phylogeny was poorly resolved, however, both trees grouped CSSD isolates within one large clade, including the newly discovered Cacao red vein virus (CRVV) proposed species. The genome arrangement of the four species consists of four, five, or six predicted open reading frames (ORFs), and the CPDs have similar architectures. By comparison, two New World cacao-infecting badnaviruses encode four ORFs, and harbor CPDs like the West African species.ConclusionsThree previously recognized West African cacao-infecting badnaviral species were identified, and a fourth, previously unidentified species, CRVV, is described for the first time. The CRVV is a suspect causal agent of the rapid decline phenotype, however Koch’s Postulates have not been proven. To reconcile viral evolutionary with epidemiology considerations, more detailed information about CSSD-genomic variability is essential. Also, the functional basis for the multiple genome arrangements and subtly distinct CPD architectures among cacao-infecting badnaviruses is poorly understood. New knowledge about functional relationships may help explain the diverse symptomatologies observed in affected cacao trees.Electronic supplementary materialThe online version of this article (10.1186/s12985-017-0866-6) contains supplementary material, which is available to authorized users.

A Complex of Badnavirus Species Infecting Cacao Reveals Mixed Infections, Extensive Genomic Variability, and Interspecific Recombination

“…With the increasing number of available cacao-infecting badnavirus genome sequences, species diversity and genomic variability have been shown to be much greater than anticipated. However, this hypothesis is based on a relatively small sample size that is not representative of the entire region [10,11,15,21]. Even so, this type of genomic pattern is consistent with the non-proofreading function associated with the reverse transcriptase encoded by badnaviruses, and their potential for intra-and interspecific recombination [42,43].…”

“…Symptoms consisted of discoloration of leaves, vein chlorosis, red vein-banding, stem and root swellings, and pod deformation, with tree decline and death 3-5 years after symptoms development [6,7]. With the expansion of cacao production into other West African countries, outbreaks caused by cacao swollen shoot disease (CSSD) were reported throughout the entire region [8][9][10][11][12][13][14][15][16][17][18]. Disease symptoms reminiscent of CSSD in West Africa were observed in cacao in Sri Lanka in 1956-1957 [19]; however, only recently, the badnavirus Cacao bacilliform Sri Lanka virus (CBSLV) was identified in cacao trees showing symptoms similar to those described in the 1950s [15].…”

“…The largest is ORF3, which encodes a polyprotein comprising the viral capsid and movement protein domains, the aspartate protease responsible for polyprotein cleavage, and the reverse transcriptase (RT) and ribonuclease H (RNase H) domains involved in viral replication [24,31]. The cacao-infecting badnaviruses have one to three additional ORFs, known as ORF4, ORFX, and/or ORFY whose functions are still unknown [10,11,14,15,21,30,34].…”

“…The genome sequence of CSSTBV was the first CSSD-badnavirus to be determined and characterized [30]. Recently, additional full-length CSSD-badnaviral genomes have been determined from symptomatic cacao plants in West Africa [10,11,14,15,21,34], with ten cacao-infecting badnavirus species being presently recognized by the International Committee on Taxonomy of Viruses (ICTV; https://talk.ictvonline.org/taxonomy/): CBSLV, CaMMV, CYVBV, Cacao swollen shoot CD virus (CSSCDV), Cacao swollen shoot CE virus (CSSCEV; also known as Cacao red vein virus), Cacao swollen shoot Ghana M virus (CSSGMV; also known as Cacao red vein banding virus), Cacao swollen shoot Ghana N virus (CSSGNV), Cacao swollen shoot Ghana Q virus (CSSGQV), Cacao swollen shoot Togo A virus (CSSTAV), and CSSTBV (previously named as Cacao swollen shoot virus).…”

Insect Diversity of Cocoa (Theobroma Cacao L.) Beans Stocks From Hautsassandra Region and Their Impacts (Daloa, Cote Divoire)

“…Concerning diseases, Phytophthora and Loranthus attacks lead to significant production losses. Virus disease such as swollen shoot destroys the cocoa tree after 3 to 5 years (Chingandu et al, 2017). Stored cocoa beans are often subject to losses of a variable and complex nature, most of which are attributed to insects, micro-organisms and rodents (Kekeunou et al, 2006;Tah et al, 2016).…”