Baculovirus‐induced tree‐top disease: how extended is the role ofegtas a gene for the extended phenotype?

Abstract

Many parasites alter host behaviour to enhance their chance of transmission. Recently, the ecdysteroid UDP-glucosyl transferase (egt) gene from the baculovirus Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) was identified to induce tree-top disease in L. dispar larvae. Infected gypsy moth larvae died at elevated positions (hence the term tree-top disease), which is thought to promote dissemination of the virus to lower foliage. It is, however, unknown whether egt has a conserved role among baculoviruses in inducing tree-top disease. Here, we studied tree-top disease induced by the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) in two different host insects, Trichoplusia ni and Spodoptera exigua, and we investigated the role of the viral egt gene therein. AcMNPV induced tree-top disease in both T. ni and S. exigua larvae, although in S. exigua a moulting-dependent effect was seen. Those S. exigua larvae undergoing a larval moult during the infection process died at elevated positions, while larvae that did not moult after infection died at low positions. For both T. ni and S. exigua, infection with a mutant AcMNPV lacking egt did not change the position where the larvae died. We conclude that egt has no highly conserved role in inducing tree-top disease in lepidopteran larvae. The conclusion that egt is a 'gene for an extended phenotype' is therefore not generally applicable for all baculovirus-host interactions. We hypothesize that in some baculovirus-host systems (including LdMNPV in L. dispar), an effect of egt on tree-top disease can be observed through indirect effects of egt on moulting-related climbing behaviour.

Host miRNAs are involved in hormonal regulation of HaSNPV‐triggered climbing behaviour in Helicoverpa armigera

“…It was hypothesized that inactivation of 20E by egt disrupts the moulting cycle, inducing larvae to remain up in the tree in a feeding state, rather than crawling down to moult. Upon infection with an egt deletion virus, larvae stop feeding and might move down to moult (Hoover et al., ; Ros et al., ). A similar effect of egt on moulting‐related behaviour was seen in AcMNPV‐infected S. exigua and T. ni larvae.…”

“…These larvae normally climb to lower positions prior to moulting, and this behaviour was absent in WT AcMNPV‐infected larvae. However, in AcMNPV‐infected S. exigua and T. ni larvae, death occurred long after moulting, and climbing prior to death (tree‐top disease), which occurs at a later stage of infection, was not affected by egt (Ros et al., ).…”

“…In Helicoverpa armigera , infection by the egt ‐negative virus of H. armigera single nucleopolyhedrovirus (HaSNPV) resulted in lower virus yield and faster time to death in fourth instars; however, there was no effect on the death positions of larvae under controlled glasshouse conditions or in field cages (Georgievska et al., ). Larvae of Trichoplusia ni and Spodoptera exigua that were infected with Autographa californica multiple nucleopolyhedrovirus (AcMNPV) also died at the same height as larvae infected with a mutant virus lacking the egt gene (Ros, van Houte, Hemerik, & van Oers, ). However, climbing behaviour that occurred prior to moulting was suppressed in WT AcMNPV‐infected larvae, indicating that egt did affect climbing behaviour that was related to moulting.…”

Insect virus transmission: different routes to persistence

“…Demonstrating that pathogen-induced behavioural changes are adaptive and do increase transmission can be challenging. However, it has recently been demonstrated that the egt gene is not responsible for the climbing behaviour seen when the cabbage looper, Trichoplusia ni and S. exigua are infected by AcMNPV [27]. Research on the domesticated silkworm, Bombyx mori, showed that the protein tyrosine phosphatase (ptp) gene of its NPV was responsible for the hyperactivity of infected larvae [23].…”

Reprogramming of larval locomotory pattern during baculovirus-induced host manipulation

“…As ptp deletion affects ELA but not climbing height during AcMNPV infection, ELA and 60 CB are thought to be governed by different mechanisms [12]. The deletion of egt in Lymantria dispar 61 multiple nucleopolyhedrovirus and Spodoptera exigua multiple nucleopolyhedrovirus mitigates the 62 climbing height of Lymantria dispar and S. exigua larvae, respectively, although the enhancement of 63 larval activity by egt was not observed in BmNPV-and AcMNPV-infected larvae [9,[13][14][15]. A recent 64 study further showed that miRNA-mediated hormonal regulation affects the climbing height of 65…”