Laboratory of Virology, Embrapa Vegetables, Brasília, Federal District, Brazil.
Department of Plant Pathology, University of California- Davisgrid.27860.3b, Davis, California, USA.
J Virol. 2022 Sep 28;96(18):e0072522. doi: 10.1128/jvi.00725-22. Epub 2022 Aug 31.
Begomoviruses are members of the family , a large and diverse group of plant viruses characterized by a small circular single-stranded DNA genome encapsidated in twinned quasi-icosahedral virions. Cultivated tomato ( L.) is particularly susceptible and is infected by >100 bipartite and monopartite begomoviruses worldwide. In Brazil, 25 tomato-infecting begomoviruses have been described, most of which are bipartite. Tomato mottle leaf curl virus (ToMoLCV) is one of the most important of these and was first described in the late 1990s but has not been fully characterized. Here, we show that ToMoLCV is a monopartite begomovirus with a genomic DNA similar in size and genome organization to those of DNA-A components of New World (NW) begomoviruses. Tomato plants agroinoculated with the cloned ToMoLCV genomic DNA developed typical tomato mottle leaf curl disease symptoms, thereby fulfilling Koch's postulates and confirming the monopartite nature of the ToMoLCV genome. We further show that ToMoLCV is transmitted by whiteflies, but not mechanically. Phylogenetic analyses placed ToMoLCV in a distinct and strongly supported clade with other begomoviruses from northeastern Brazil, designated the ToMoLCV lineage. Genetic analyses of the complete sequences of 87 ToMoLCV isolates revealed substantial genetic diversity, including five strain groups and seven subpopulations, consistent with a long evolutionary history. Phylogeographic models generated with partial or complete sequences predicted that the ToMoLCV emerged in northeastern Brazil >700 years ago, diversifying locally and then spreading widely in the country. Thus, ToMoLCV emerged well before the introduction of MEAM1 whiteflies, suggesting that the evolution of NW monopartite begomoviruses was facilitated by local whitefly populations and the highly susceptible tomato host. Worldwide, diseases of tomato caused by whitefly-transmitted geminiviruses (begomoviruses) cause substantial economic losses and a reliance on insecticides for management. Here, we describe the molecular and biological properties of tomato mottle leaf curl virus (ToMoLCV) from Brazil and establish that it is a NW monopartite begomovirus indigenous to northeastern Brazil. This answered a long-standing question regarding the genome of this virus, and it is part of an emerging group of these viruses in Latin America. This appears to be driven by widespread planting of the highly susceptible tomato and by local and exotic whiteflies. Our extensive phylogenetic studies placed ToMoLCV in a distinct strongly supported clade with other begomoviruses from northeastern Brazil and revealed new insights into the origin of Brazilian begomoviruses. The novel phylogeographic analysis indicated that ToMoLCV has had a long evolutionary history, emerging in northeastern Brazil >700 years ago. Finally, the tools used here (agroinoculation system and ToMoLCV-specific PCR test) and information on the biology of the virus (host range and whitefly transmission) will be useful in developing and implementing integrated pest management (IPM) programs targeting ToMoLCV.
番茄曲叶病毒是双生病毒科的一个成员，该科是一个具有很大多样性的植物病毒科，其特征是具有一个小型环状单链 DNA 基因组，被包装在孪生准二十面体病毒粒子中。栽培番茄（L.）特别易感，并且在全球范围内受到 100 多种二分体和单分体番茄曲叶病毒的感染。在巴西，已经描述了 25 种感染番茄的曲叶病毒，其中大多数是二分体的。番茄斑驳卷曲病毒（ToMoLCV）是其中最重要的一种，它于 20 世纪 90 年代末首次被描述，但尚未得到充分表征。在这里，我们表明 ToMoLCV 是一种单分体的曲叶病毒，其基因组 DNA 的大小和基因组组织与新世界（NW）曲叶病毒的 DNA-A 组分相似。用克隆的 ToMoLCV 基因组 DNA agroinoculated的番茄植物表现出典型的番茄斑驳卷曲病症状，从而满足了科赫的假设，并证实了 ToMoLCV 基因组的单分体性质。我们进一步表明，ToMoLCV 可以通过粉虱传播，但不能通过机械传播。系统发育分析将 ToMoLCV 置于与来自巴西东北部的其他曲叶病毒密切相关且得到有力支持的分支中，称为 ToMoLCV 谱系。对 87 个 ToMoLCV 分离物的完整序列的遗传分析显示出相当大的遗传多样性，包括五个株系组和七个亚种群，这与长期的进化历史相一致。使用部分或完整序列生成的系统发育模型预测，ToMoLCV 是在 700 多年前在巴西东北部出现的，在当地多样化，然后在全国范围内广泛传播。因此，ToMoLCV 的出现远早于 MEAM1 粉虱的引入，这表明 NW 单分体曲叶病毒的进化是由当地粉虱种群和高度易感的番茄宿主促成的。 在全球范围内，由粉虱传播的双生病毒（曲叶病毒）引起的番茄病害会造成重大的经济损失，并依赖杀虫剂进行管理。在这里，我们描述了来自巴西的番茄斑驳卷曲病毒（ToMoLCV）的分子和生物学特性，并确定它是一种源自巴西东北部的 NW 单分体曲叶病毒。这回答了关于该病毒基因组的一个长期存在的问题，并且它是拉丁美洲新兴的曲叶病毒群的一部分。这似乎是由高度易感的番茄的广泛种植以及当地和外来粉虱驱动的。我们广泛的系统发育研究将 ToMoLCV 置于与来自巴西东北部的其他曲叶病毒密切相关且得到有力支持的分支中，并揭示了巴西曲叶病毒起源的新见解。新的系统地理分析表明，ToMoLCV 具有悠久的进化历史，于 700 多年前在巴西东北部出现。最后，这里使用的工具（农杆菌接种系统和 ToMoLCV 特异性 PCR 测试）和关于病毒生物学的信息（宿主范围和粉虱传播）将有助于制定和实施针对 ToMoLCV 的综合虫害管理（IPM）计划。
