Outcome of virus–host–vector interactions may vary depending on the specific virus–host–vector combination and probably other factors (Mauck & Chesnais, 2020 Mauck et al., 2018).Ĭauliflower mosaic virus (CaMV) (genus Caulimovirus, family Caulimoviridae) has features of nonpersistent and persistent viruses and is often classified as a semipersistent virus. While many reports support these models, there are also a number of examples that do not follow the expectations. Vector departure is often related to the poor taste and low nutritive value of infected plants (Mauck et al., 2014). Plants infected with noncirculative and nonpersistent viruses may attract vectors for virus acquisition (Fereres & Moreno, 2009) and subsequently encourage them to leave the plants rapidly for fast dispersal of the virus, as shown for cucumber mosaic virus (Mauck et al., 2010).
In contrast, noncirculative and nonpersistent viruses are often tissue generalists, with fast acquisition and short retention times. The circulative and persistent viruses also tend to increase food quality of the host, resulting in an improvement in vector fitness and an increase in vector population (Dáder et al., 2017 Fereres & Moreno, 2009 Mauck et al., 2018). General predictions assume that these viruses would benefit from fast and prolonged access of vectors to the phloem, which would facilitate virus acquisition.
Circulative and persistent viruses are most often phloem-restricted and characterized by long acquisition and retention times in the vector, resulting in prolonged, often lifelong transmissibility. Transmission modes are classified by two criteria: retention time in the vector (persistence) and vector interaction, with circulative viruses cycling through the vector body before being inoculated as a saliva component into a new host plant and noncirculative viruses interacting only with the vector mouthparts. The ways viruses modify or even manipulate plant hosts and vectors depend on the transmission mode and tissue tropism of the virus (Mauck et al., 2012). The interactions may be direct, that is, changes in vector behaviour or fitness following virus acquisition by and retention in the vector, or indirect, that is, plant traits like odour, colour, and nutritive value modified by viral infection impact vector behaviour and fitness (for review see Dáder et al., 2017 Fereres & Moreno, 2009 Mauck et al., 2018). Evidence accumulates that viruses interact with both hosts and vectors and alter some of their characteristics to optimize transmission. Among these, insects with a piercing-sucking feeding behaviour such as aphids are the most efficient vectors, because they can, with great precision and without inflicting major damage to plant cells, acquire and inoculate viruses in distinct plant tissues. Most plant viruses rely on arthropod vectors for their transmission to a new host. Taken together, we show that CaMV infection can modify both aphid fecundity and feeding behaviour and that P6 is only involved in the latter. Analysis of plants expressing P6 mutants identified N-terminal P6 domains contributing to modification of feeding behaviour. Aphid feeding behaviour was modified on wt P6-CM-, but not on wt P6-JI-expressing plants. In contrast to viral infection, aphid fecundity was unchanged on all transgenic lines, suggesting that other viral factors compromise fecundity. To evaluate the role of the multifunctional CaMV protein P6-TAV, aphid feeding behaviour and fecundity were tested on transgenic Arabidopsis plants expressing wild-type (wt) and mutant versions of P6-TAV.
Compared to mock-inoculated plants, feeding behaviour was altered similarly on CM- and JI-infected plants, but only aphids on JI-infected plants had reduced fecundity. Here we compared the effects of Arabidopsis infection with mild (CM) and severe (JI) CaMV isolates on the feeding behaviour (recorded by the electrical penetration graph technique) and fecundity of the aphid vector Myzus persicae. Similar evidence for semipersistent viruses like cauliflower mosaic virus (CaMV) is scarce. Emerging evidence suggests that viral infection modifies host plant traits that in turn alter behaviour and performance of vectors colonizing the plants in a way conducive for transmission of both nonpersistent and persistent viruses.
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