PHIM Plant Health Institute, University of Montpellier, INRAE, CIRAD, IRD, Institute Agro, Montpellier, France.
Faculté des Sciences Agronomiques, Université Pédagogique Nationale, Kinshasa, Democratic Republic of the Congo.
PLoS Pathog. 2022 Apr 12;18(4):e1010448. doi: 10.1371/journal.ppat.1010448. eCollection 2022 Apr.
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.
香蕉束顶病毒（BBTV）是一种六组分 ssDNA 病毒（属 Babuvirus，家族 Nanoviridae），通过蚜虫传播，感染单子叶植物（主要是 Musaceae 科的物种），可能起源于东南亚，在那里它经常与自我复制的α卫星相伴。对来自非洲的香蕉蚜虫和叶片样本的 Illumina 测序分析揭示了一种α卫星，它应归类于一个新属，在系统发育上与感染双子叶植物的纳米病毒的α卫星相关。α卫星 DNA 被 BBTV 衣壳蛋白包裹，并在植物和蚜虫中高水平积累，从而降低辅助病毒的载量，改变病毒基因组成分的相对丰度（公式），并干扰蚜虫传播病毒。BBTV 和α卫星克隆感染双子叶植物 Nicotiana benthamiana，随后恢复并无症状地持续存在α卫星和 BBTV 复制蛋白（Rep），但不是α卫星 Rep，诱导叶片黄化。转录组测序揭示了 21、22 和 24 个核苷酸的小干扰（si）RNA，覆盖整个病毒基因组的双链，病毒 mRNA 的单方向 Pol II 转录单位，以及每个成分和α卫星的双向广泛转录，可能产生病毒 siRNA 的双链前体。与后一种假说一致，带有和不带有α卫星的病毒 DNA 公式类似于病毒 siRNA 公式，但不同于 mRNA 公式。α卫星降低了编码假定的蚜虫传播因子的 DNA-N 的转录效率，并增加了 Rep 和运动蛋白编码成分的相对 siRNA 产生率。α卫星本身产生了最丰富的 siRNA，并且具有最低的 mRNA 转录率。总的来说，在非洲入侵之后，BBTV 与一种可能来自双子叶植物的α卫星相关联，并干扰了 BBTV 的复制和传播。受感染香蕉植物的病毒分子分析揭示了病毒 DNA 转录和 siRNA 生物发生的新特征，这两者都受到α卫星的影响。讨论了α卫星与辅助病毒关联的成本和收益。
