Direct and Indirect Effect via Endophytism of Entomopathogenic Fungi on the Fitness of Myzus persicae and Its Ability to Spread PLRV on Tobacco

SIMPLE SUMMARY: Aphids are major crop pests that are feeding on plant sap and transmitting plant viruses, thus inducing high yield losses worldwide. As chemical pesticides are decreasingly used in plant protection, fungi that cause disease to insects (entomopathogenic fungi) are one of the promising alternatives. They are commonly applied by spraying plants to protect them against herbivores. When applied, some fungi penetrate and live within plant tissues, thus helping to internally protect from insect attacks and other plant diseases. The aim of our study was to assess the effects of entomopathogenic fungi (EPF) applied firstly by contact after insect direct spraying, secondly by endophytic plant inoculation, and thirdly by associated both methods assessing the green peach aphid performances. The impact of the presence of endophytic entomopathogenic fungi (EEPF) in plant tissues on virus transmission by aphids was also considered. We found that the EPF Beauveria bassiana killed the green peach aphid and reduced its fecundity regardless of the application method. On fungal-inoculated plants, there was also a high mortality of aphid nymphs and infection by the potato leafroll virus (PLRV) was delayed by about a week with the EEPF treatment compared to fungal-free plants. This study showed that spraying plant leaves with EPF not only has a direct insecticidal effect against insects but could also have beneficial side effects for the plant against viruses. ABSTRACT: Aphids are major crop pests that transmit more than half of all insect-vectored plant viruses responsible for high yield losses worldwide. Entomopathogenic fungi (EPF) are biological control agents mainly used by foliar application to control herbivores, including sap-sucking pests such as aphids. Their ability to colonize plant tissues and to interact with diverse plant pathogenic microorganisms have been reported. In our study, we evaluated the effectiveness of Beauveria bassiana ((Balsamo-Crivelli) Vuillemin) directly applied by contact or/and indirectly via endophytism in tobacco plants (Nicotiana tabacum L.) against the virus vector Myzus persicae (Sulzer) carrying the Potato leafroll virus (PLRV) or not. We found that both contact treatment and endophytic colonization of leaves significantly increased aphid mortality and decreased the fecundity rate when compared to control plants. In addition, on fungal-colonized leaves, viruliferous aphids were more negatively impacted than virus-free ones and nymph mortality was significantly higher than on fungal-free plants. Furthermore, we assessed PLRV transmission by M. persicae on tobacco plants inoculated with either B. bassiana or Metarhizium acridum ((Driver and Milner) JF Bischoff, Rehner, and Humber) as source or/and recipient plants. Myzus persicae was found to acquire and transmit PLRV regardless of the treatment. Nevertheless, the infection rate of endophytically colonized plants was lower at a seven-day incubation period and had increased to almost 100% after fifteen days. These results suggest that B. bassiana is effective against aphids, both by contact and via endophytism, and both B. bassiana and M. acridum delayed PLRV infection in tobacco.