How tobacco mosaic virus goes the distance.

Abstract

Human viruses are the current focus of many virologists worldwide. However, the first virus that was discovered was a plant virus. In the nineteenth century, several researchers were investigating a disease in tobacco plants that caused mottled browning of leaves (Rifkind and Freeman, 2005). The Russian microbiologist Dmitry Ivanovsky found that this disease was caused by something so small that it was able to pass through a filter with pores that could hold back bacteria. Later, the Dutch botanist Willem Beijerinck showed that the disease-causing agent was ‘alive’ and self-replicating rather than a chemical toxin. The virus, now called tobacco mosaic virus (TMV), is still of major concern because—despite its name—it causes disease in a wide range of plants, including tomato (Solanum lycopersicum), cucumber (Cucumis sativus), and several ornamental flowers. The infectious virus particle—or virion—of TMV is composed of a single strand of RNA covered by a protein shell (capsid) that assembles into a rod-shaped structure. The capsid is entirely made up of subunits of a single protein, called coat protein. Without it, the virus is not able to form a virion. Virion assembly was long thought to play important roles in other aspects, such as the ability to move systemically through the phloem of the plant to reach distal tissues. Indeed, previous research showed that the virus is not able to move over long distances without the coat protein (Saito et al., 1990). However, more recent findings indicate the coat protein also has a function in the systemic movement of the virus that is not linked with the formation of virions (Bendahmane et al., 2007). In this issue, researchers from the Instituto de Agrobiotecnología y Biología Molecular, Argentina investigated how the coat protein of TMV facilitates long-distance movement (Venturuzzi et al., 2021). For this purpose, they used a mutant virus that lacks the gene encoding the coat protein and therefore cannot move systemically. When inoculated with the mutant virus, only a low number of plants accumulated the virus in tissues distal to the infection site. But when the authors co-inoculated the mutant virus with a vector encoding the coat protein (to complement the mutation), the virus was able to move systemically in most plants. Furthermore, when they inoculated one leaf with the virus and another, distal leaf with the coat protein-encoding vector, they observed long-distance movement as well. This indicates that the coat protein allows long-distance movement independent from virion formation. The salicylic acid (SA)-mediated defense response is a key pathway involved in the restriction of systemic infections in plants. Therefore, the authors investigated the role of this defense pathway in the long-distance movement of TMV by performing experiments with several SA-pathway mutants. This drew their attention towards NON-EXPRESSER OF PR GENES 1 (NPR1) and the TGACG-binding transcription factor TGA10. When they infected plant mutants of these genes with wild-type virus, they noticed that the virus accumulated at a higher level than in wild-type plants. Moreover, comparisons of gene expression levels of infected and non-infected plants showed that several genes that are downregulated by the coat protein in wild-type plants show a different expression pattern in npr1/tga10 mutant plants. This indicates that NPR1 and TGA10 might be involved in repressing viral movement upon recognition of the capsid protein. To test this hypothesis, the authors performed infection experiments in NPR1- and TGA10-silenced plants with a mutant virus that lacks the coat protein. In most of these plants, systemic movement of the mutant virus was observed. Previous studies from the same research group showed that the coat protein can stabilize DELLA transcription factors. As TGA10 is known to interact with DELLAs, the authors decided to investigate if these transcription factors are also involved in systemic movement of the virus. They found that overexpression of GIBBERELLIC ACID INSENSITIVE (GAI) allowed the systemic movement of the coat protein-deficient mutant. The same was true for plants in which DELLAs were stabilized through the application of the GA biosynthesis inhibitor Paclobutrazol. This indicates that DELLAs facilitate systemic movement, potentially through stabilization by the coat protein. The authors constructed a model to explain the roles of NPR1, TGA transcription factors, and DELLA proteins together with several other defense-related proteins that are involved in the systemic movement of TMV (Figure ). The corresponding author Sebastian Asurmendi explains that in the future, he aims to study these different players in more detail to establish their molecular functions. He is especially interested in understanding how the coat protein stabilizes DELLAs. DELLA proteins are involved in many physiological and developmental plant processes, and therefore a target for plant breeders. That they also play a role in viral movement implies that genetic manipulations of DELLAs might also affect plant immunity. For now, good advice for breeders targeting DELLAs: test how the plants respond to viral infection.