Prothoracicotropic Hormone Acts as a Neuroendocrine Switch between Pupal Diapause and Adult Development

Abstract

Diapause is a programmed developmental arrest that has evolved in a wide variety of organisms and allows them survive unfavorable seasons. This developmental state is particularly common in insects. Based on circumstantial evidence, pupal diapause has been hypothesized to result from a cessation of prothoracicotropic hormone (PTTH) secretion from the brain. Here, we provide direct evidence for this classical hypothesis by determining both the PTTH titer in the hemolymph and the PTTH content in the brain of diapause pupae in the cabbage army moth Mamestra brassicae. For this purpose, we cloned the PTTH gene, produced PTTH-specific antibodies, and developed a highly sensitive immunoassay for PTTH. While the hemolymph PTTH titer in non-diapause pupae was maintained at high levels after pupation, the titer in diapause pupae dropped to an undetectable level. In contrast, the PTTH content of the post-pupation brain was higher in diapause animals than in non-diapause animals. These results clearly demonstrate that diapause pupae have sufficient PTTH in their brain, but they do not release it into the hemolymph. Injecting PTTH into diapause pupae immediately after pupation induced adult development, showing that a lack of PTTH is a necessary and sufficient condition for inducing pupal diapause. Most interestingly, in diapause-destined larvae, lower hemolymph titers of PTTH and reduced PTTH gene expression were observed for 4 and 2 days, respectively, prior to pupation. This discovery demonstrates that the diapause program is already manifested in the PTTH neurons as early as the mid final instar stage.

Identification of ecdysteroidogenic enzyme genes and their expression during pupal diapause in the cabbage armyworm, Mamestra brassicae

“…These changes in ecdysteroid titres regulate the preparation for moulting or metamorphosis. In contrast, increases in ecdysteroid titres are rarely observed in insects during diapause, when moulting and metamorphosis do not occur (Denlinger et al ., ; Mizoguchi et al ., ). In addition, artificial depletion of ecdysteroid titres by a fungal ecdysteroid‐inactivating enzyme mimics the developmental arrest of the diapause of Haritalodes basipunctali (Kamimura et al ., ).…”

“…The role of ecdysteroidogenic enzymes in diapause has not been well studied compared with regular development, although it has been shown that ecdysteroid titres in the haemolymph are considerably reduced during diapause (Endo et al ., ; Mizoguchi et al ., ; Denlinger et al ., ). To elucidate how ecdysteroidogenic enzymes contribute to low ecdysteroid concentrations during diapause, we determined gene expression profiles of these enzymes during diapause.…”

Identification of the prothoracicotropic hormone (Ptth) coding gene and localization of its site of expression in the pea aphid Acyrthosiphon pisum

“…PTTH thus plays a key role in the control of moulting and metamorphosis and, consequently, in the transition from juvenile to adult stages. Moreover, both PTTH release or blockade have been reported to act as a switch to terminate or initiate larval and pupal diapauses (Zhang & Denlinger, ; Bloch et al ., ; Mizoguchi et al ., ; Wang et al ., ; De Loof et al ., ). Diapause is very often a response triggered by day length (photoperiod) variation (Saunders, ; Nelson et al ., ; Koštál, ; Hand et al ., ).…”

Artemin, a Diapause-Specific Chaperone, Contributes to the Stress Tolerance of Artemia Cysts and Influences Their Release from Females

“…Diapause, which is most common in insects (Poelchau et al, 2013;Mizoguchi et al, 2013;Fan et al, 2013) but occurs in organisms as diverse as rotifers (Clark et al, 2012), tardigrades (Guidetti et al, 2011), crustaceans (Tarrant et al, 2008;King and MacRae, 2012;Clark et al, 2013), killifish (Meller et al, 2012) and mammals (Murphy, 2012;Cha et al, 2013), entails decreased metabolism and augmentation of stress tolerance (Denlinger, 2002;Koštál, 2006;MacRae, 2010;Hahn and Denlinger, 2011). Photoperiod, temperature and crowding induce diapause, an integral part of the life cycle of many animals (Xiao et al, 2010;Meuti and Denlinger, 2013).…”