Cryptochromes and Hormone Signal Transduction under Near-Zero Magnetic Fields: New Clues to Magnetic Field Effects in a Rice Planthopper

Abstract

Although there are considerable reports of magnetic field effects (MFE) on organisms, very little is known so far about the MFE-related signal transduction pathways. Here we establish a manipulative near-zero magnetic field (NZMF) to investigate the potential signal transduction pathways involved in MFE. We show that exposure of migratory white-backed planthopper, Sogatella furcifera, to the NZMF results in delayed egg and nymphal development, increased frequency of brachypterous females, and reduced longevity of macropterous female adults. To understand the changes in gene expression underlying these phenotypes, we examined the temporal patterns of gene expression of (i) CRY1 and CRY2 as putative magnetosensors, (ii) JHAMT, FAMeT and JHEH in the juvenile hormone pathway, (iii) CYP307A1 in the ecdysone pathway, and (iv) reproduction-related Vitellogenin (Vg). The significantly altered gene expression of CRY1 and CRY2 under the NZMF suggest their developmental stage-specific patterns and potential upstream location in magnetic response. Gene expression patterns of JHAMT, JHEH and CYP307A1 were consistent with the NZMF-triggered delay in nymphal development, higher proportion of brachypterous female adults, and the shortened longevity of macropterous female adults, which show feasible links between hormone signal transduction and phenotypic MFE. By conducting manipulative NZMF experiments, our study suggests an important role of the geomagnetic field (GMF) in modulating development and physiology of insects, provides new insights into the complexity of MFE-magnetosensitivity interactions, and represents an initial but crucial step forward in understanding the molecular basis of cryptochromes and hormone signal transduction involved in MFE.

Geomagnetic field absence reduces adult body weight of a migratory insect by disrupting feeding behavior and appetite regulation

“…Following the previously used workflow and standards for one generation of exposure of rice planthoppers (Wan et al, 2015b). We exposed N. lugens individuals to NZMF vs. GMF conditions for either one generation (from mated F0 females to newly emerged F1 adults) or less than one generation (from mated F0 females to older nymphs) because their long-distance migration is usually initiated after adults emerge following at least one generation of local reproduction (Cheng et al, 2003).…”

“…Instar durations to the adult stage (instars 1-5) were measured in days as previously described for the white-backed planthopper, Sogatella furcifera (Wan et al, 2015b). Differentiating between the sexes of juveniles is very difficult and was not attempted for the molecular, behavioral, and biochemical assays of nymphs described below.…”

“…In a narrow sense, magnetoreception refers to the acute ability of animals to detect the GMF (Lohmann, 2010). However, increasing evidence for chronic responses of organisms to magnetic field variation suggests the importance of general magnetoreception in biological processes across taxa (Binhi and Prato, 2017;Henshaw et al, 2009;Maffei, 2014;Wan et al, 2016;Wan et al, 2014;Wan et al, 2015b;Wang et al, 2008). Among studies that subject organisms to different magnetic field intensity treatments, many concern the bioeffects induced by the near-zero magnetic field (NZMF) (Binhi and Prato, 2017;Wang et al, 2008).…”

“…Studies of three closely related species of migratory rice planthoppers, Nilaparvata lugens, Laodelphax striatellus and Sogatella furcifera, have shown that the absence of the GMF (i.e., the NZMF) affects a number of physiological and behavioral processes such as nymphal development, adult longevity, body weight, wing dimorphism, positive phototaxis, and flight behaviors, potentially through Cry-mediated hormone signaling Wan et al, 2014;Wan et al, 2015b).…”

Geomagnetic field intensity as a cue for the regulation of insect migration

“…Our work with migratory white-backed planthopper, Sogatella furcifera , showed that the absence of GMF can affect the expression of important migration-related behaviours, potentially through Cry-mediated hormone signaling. This includes changes in positive phototaxis which is critical for the ascent process, and flight capacity which is energetically-intensive and one of the main parameters used to assess migration ability [9, 18]. Additionally, previous work in migratory birds showed that changes in GMF information (both intensity and direction) over the migration route can affect their fuelling decisions and migratory restlessness [19-22].…”