SVQV, UMR 1131, INRAE Centre Grand Est, Colmar, France.
Université Strasbourg, Strasbourg, France.
Microbiol Spectr. 2024 Nov 5;12(11):e0111524. doi: 10.1128/spectrum.01115-24. Epub 2024 Oct 10.
Multi-infection of plants by viruses is very common and can change drastically infection parameters such as virus accumulation, distribution, and vector transmission. Sugar beet is an important crop that is frequently co-infected by the polerovirus beet chlorosis virus (BChV) and the closterovirus beet yellows virus (BYV), both vectored by the green peach aphid (). These phloem-limited viruses are acquired while aphids ingest phloem sap from infected plants. Here we found that co-infection decreased transmission of BChV by ~50% but had no impact on BYV transmission. The drastic reduction of BChV transmission was due to neither lower accumulation of BChV in co-infected plants nor reduced phloem sap ingestion by aphids from these plants. Using the signal amplification by exchange reaction fluorescent hybridization technique on plants, we observed that 40% of the infected phloem cells were co-infected and that co-infection caused redistribution of BYV in these cells. The BYV accumulation pattern changed from distinct intracellular spherical inclusions in mono-infected cells to a diffuse form in co-infected cells. There, BYV co-localized with BChV throughout the cytoplasm, indicative of virus-virus interactions. We propose that BYV-BChV interactions could restrict BChV access to the sieve tubes and reduce its accessibility for aphids and present a model of how co-infection could alter BChV intracellular movement and/or phloem loading and reduce BChV transmission.IMPORTANCEMixed viral infections in plants are understudied yet can have significant influences on disease dynamics and virus transmission. We investigated how co-infection with two unrelated viruses, BChV and BYV, affects aphid transmission of the viruses in sugar beet plants. We show that co-infection reduced BChV transmission by about 50% without affecting BYV transmission, despite similar virus accumulation rates in co-infected and mono-infected plants. Follow-up experiments examined the localization and intracellular distribution of the viruses, leading to the discovery that co-infection caused a redistribution of BYV in the phloem vessels and altered its repartition pattern within plant cells, suggesting virus-virus interactions. In conclusion, the interplay between BChV and BYV affects the transmission of BChV but not BYV, possibly through direct or indirect virus-virus interactions at the cellular level. Understanding these interactions could be crucial for managing virus propagation in crops and preventing yield losses.
植物的多病毒感染非常普遍，会极大地改变病毒积累、分布和载体传播等感染参数。甜菜是一种重要的作物，经常同时感染极细病毒属的甜菜褪绿病毒（BChV）和联体病毒属的甜菜黄化病毒（BYV），这两种病毒都由桃蚜（）传播。这些韧皮部限制的病毒是蚜虫在吸食感病植物的韧皮部汁液时获得的。在这里，我们发现共感染使 BChV 的传播减少了约 50%，但对 BYV 传播没有影响。BChV 传播的急剧减少既不是由于共感染植物中 BChV 的积累减少，也不是由于蚜虫从这些植物中摄取的韧皮部汁液减少。我们使用植物上的交换反应荧光杂交技术信号放大，观察到 40%的感染韧皮部细胞被共感染，共感染导致这些细胞中的 BYV 重新分布。BYV 的积累模式从单感染细胞中的明显细胞内球形内含物变为共感染细胞中的弥散形式。在那里，BYV 与 BChV 共定位在细胞质中，表明病毒-病毒相互作用。我们提出，BYV-BChV 相互作用可能会限制 BChV 进入筛管的途径，并降低蚜虫对其的易感性，并提出了一个模型，说明共感染如何改变 BChV 的细胞内运动和/或韧皮部装载，并降低 BChV 的传播。重要性植物中的混合病毒感染研究不足，但对疾病动态和病毒传播有重大影响。我们研究了甜菜植株中两种不相关病毒 BChV 和 BYV 的共感染如何影响蚜虫对病毒的传播。我们表明，尽管共感染和单感染植物中的病毒积累率相似，但共感染使 BChV 的传播减少了约 50%，而 BYV 的传播不受影响。后续实验检查了病毒的定位和细胞内分布，导致发现共感染导致 BYV 在韧皮部血管中的重新分布，并改变了其在植物细胞内的分布模式，表明存在病毒-病毒相互作用。总之，BChV 和 BYV 之间的相互作用影响 BChV 的传播，但不影响 BYV 的传播，可能是通过细胞水平上的直接或间接病毒-病毒相互作用。了解这些相互作用对于管理作物中的病毒传播和防止产量损失可能至关重要。
