Abstract
Badnaviruses are double‐stranded DNA pararetroviruses of the family Caulimoviridae. Badnaviral sequences found in banana are distributed over three main clades of the genus Badnavirus and exhibit wide genetic diversity. Interestingly, the nuclear genome of many plants, including banana, is invaded by numerous badnaviral sequences although badnaviruses do not require an integration step to replicate, unlike animal retroviruses. Here, we confirm that banana streak viruses (BSVs) are restricted to clades 1 and 3. We also show that only BSVs from clade 3 encompassing East African viral species are not integrated into Musa genomes, unlike BSVs from clade 1. Finally, we demonstrate that sequences from clade 2 are definitively integrated into Musa genomes with no evidence of episomal counterparts; all are phylogenetically distant from BSVs known to date. Using different molecular approaches, we dissected the coevolution between badnaviral sequences of clade 2 and banana by comparing badnavirus integration patterns across a banana sampling representing major Musa speciation events. Our data suggest that primary viral integrations occurred millions of years ago in banana genomes under different possible scenarios. Endogenous badnaviral sequences can be used as powerful markers to better characterize the Musa phylogeny, narrowing down the likely geographical origin of the Musa ancestor.
Highlights
To gain a better overview of the presence/spread of clade 2 badnaviral sequences in banana genomes over evolutionary time, we looked for clade 2 banana endogenous viruses (BEV) in diploid banana plants representing subspecies of M. acuminata and M. balbisiana, as well as other species from the genus Musa and the two other genera of Musaceae (Ensete and Musella)
We show that some BEV sequences are shared between M. acuminata and M. balbisiana genomes
We demonstrate here for the first time that several BEVs are integrated in other species of the genus Musa, that is, M. basjoo, M. itinerans, M. laterita, M. ornata, and M. schizocarpa, but not in more phylogenetically distant samples corresponding to Callimusa and Australimusa sections or other genera of the family Musaceae (Table 3 and data not shown)
Summary
Integration is not a requisite in the life cycle of pararetroviruses, integrated pararetrovirus sequences do occur in the nuclear genomes of several plant species, including banana (Harper et al, 1999; Lockhart & Jones, 2000; Ndowora et al, 1999), citrus (Yu et al, 2019), dahlia (Pahalawatta et al, 2008), fig (Laney et al., 2012), grape (Bertsch et al, 2009), petunia (Richert-Poggeler et al, 2003), pineapple (Gambley et al, 2008), potato (Hansen et al, 2005), rice (Kunii et al, 2004), tobacco, and tomato (Gregor et al, 2004; Jakowitsch et al, 1999; Staginnus et al, 2007). Regardless of symptoms, contained all five BSV sequences belonging to clade 2 (Table 2) Their systematic presence in every EAH AAA banana tested suggests that sequences from all five species are probably integrated into the M. acuminata genome. Probes corresponding to BSUDV and BSUFV (clade 2), and BSUIV, BSULV, and BSUMV (clade 3) were hybridized to undigested and digested genomic DNA of three banana samples with symptoms and three samples without symptoms (Figures 2, S1, and S2) representative of the whole EAH AAA diversity. We observed high molecular weight signals on undigested DNA (>15 kb) without the two lower bands (open circular/supercoiled viral dsDNA, cf Figure 2a) associated with multiple band patterns; the cumulative size of all bands was >7 kb per sample on digested DNA This result indicates that BSUDV is integrated into the genomes of all genotypes tested except PKW. Corroborating PCR amplification results, the three remaining probes (BEV-UD, -P, and -Q) exhibited very striking pattern differences between M. acuminata and M. balbisiana samples, with BEV UD hybridizing only with M. acuminata individuals (Figure 5d), and BEV P (Figure 5h) and Q (Figure 5i) probes hybridizing only with M. balbisiana samples
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