A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids

Abstract

Banana bunchy top virus (BBTV) is a six-component ssDNA virus (genus Babuvirus, family Nanoviridae) transmitted by aphids, infecting monocots (mainly species in the family Musaceae) and likely originating from South-East Asia where it is frequently associated with self-replicating alphasatellites. Illumina sequencing analysis of banana aphids and leaf samples from Africa revealed an alphasatellite that should be classified in a new genus, phylogenetically related to alphasatellites of nanoviruses infecting dicots. Alphasatellite DNA was encapsidated by BBTV coat protein and accumulated at high levels in plants and aphids, thereby reducing helper virus loads, altering relative abundance (formula) of viral genome components and interfering with virus transmission by aphids. BBTV and alphasatellite clones infected dicot Nicotiana benthamiana, followed by recovery and symptomless persistence of alphasatellite, and BBTV replication protein (Rep), but not alphasatellite Rep, induced leaf chlorosis. Transcriptome sequencing revealed 21, 22 and 24 nucleotide small interfering (si)RNAs covering both strands of the entire viral genome, monodirectional Pol II transcription units of viral mRNAs and pervasive transcription of each component and alphasatellite in both directions, likely generating double-stranded precursors of viral siRNAs. Consistent with the latter hypothesis, viral DNA formulas with and without alphasatellite resembled viral siRNA formulas but not mRNA formulas. Alphasatellite decreased transcription efficiency of DNA-N encoding a putative aphid transmission factor and increased relative siRNA production rates from Rep- and movement protein-encoding components. Alphasatellite itself spawned the most abundant siRNAs and had the lowest mRNA transcription rate. Collectively, following African invasion, BBTV got associated with an alphasatellite likely originating from a dicot plant and interfering with BBTV replication and transmission. Molecular analysis of virus-infected banana plants revealed new features of viral DNA transcription and siRNA biogenesis, both affected by alphasatellite. Costs and benefits of alphasatellite association with helper viruses are discussed.

The aphidPentalonia nigronervosa(Hemiptera: Aphididae) takes advantage from the quality change in banana plant associated withBanana bunchy top virusinfection

“…The BBTV is currently reported in Africa, Asia, and Australia, while the vector is present in all banana-growing regions, even where BBTV is not yet reported (CABI 2022a, 2022b). This virus belongs to the family Nanoviridae and the genus Babuvirus , with a capsid possessing multicomponent circular single-stranded DNA genomes encapsulated in small (18–20 nm) isometric particles (Burns et al 1995, Timchenko and Bernadi 2007, Stainton et al 2015, Mukwa et al 2016, Guyot et al 2022).…”

Comparative RNA-seq analysis of resistant and susceptible banana genotypes reveals molecular mechanisms in response toBanana bunchy top virus(BBTV)

“…Although no direct link has been established on how BBTV utilizes these host TFs via effectors, previous research shows that the association of betasatellites (βC1) with Tomato yellow leaf curl China virus (TYLCCNV) increased viral pathogenicity by binding to several transcription factors that regulate plant defense responses 95 . Recently, it was reported that a self-replicating alphasatellite associated with BBTV contributes to viral replication, transcription, siRNA synthesis, and transmission 96 . Thus, more research may be undertaken to determine if the BBTV-associated alphasatellite interacts with the host's TFs to enhance viral pathogenicity in banana.…”

Reassortments in single-stranded DNA multipartite viruses: Confronting expectations based on molecular constraints with field observations

“…Nanovirus alpha-satellites are not believed to contribute any function to the other genome components as they do not trans-replicate segments of the helper virus ( Timchenko et al. 1999 ); instead, they rely on it for encapsidation, movement, and transmission ( Guyot et al. 2022 ; Mansourpour et al.…”

“…Nonetheless, the absence of DNA-N in a field isolate has been reported ( Fu et al. 2009 ), and symptoms were observed in two plants obtained under laboratory conditions, following aphid inoculation, where this segment remained undetected ( Guyot et al. 2022 ).…”