Parental silencing of a horizontally transferred carotenoid desaturase gene causes a reduction of red pigment and fitness in the pea aphid

Abstract

BACKGROUND: Aphids obtained carotenoid biosynthesis genes via horizontal gene transfers from fungi. However, the roles of these genes in the contributions of in aphids'adaptation and whether these genes could be used as RNAi-based pest control targets are not yet clear. Thus, in this study we used parental RNAi to analyze the potential function of a carotenoid desaturase gene (CdeB) by combined molecular and chemical approaches in the pea aphid (Acyrthosiphon pisum).RESULTS: Transcriptional analyses showed that CdeB was significantly more highly expressed in the red morphs compared to the green ones and was associated with the production of red carotenoid. Co-transferring of pET28a-CdeB (the CdeB gene was cloned into pET28a) and pACCRT-EIB (produced lycopene) showed a deep red color in the bacterial precipitate and produced more of a red pigment, lycopene, in vitro. Parental gene-silencing of CdeB resulted in a lower body color intensity in the treated aphids and following generations in vivo. Interestingly, the dsCdeB treatment also reduced aphid performance as reflected by a delay in nymphal developmental duration, lower weight, smaller number, and altered age structure of the population.CONCLUSION: Our results demonstrate that CdeB is involved in red color formation and the silencing of this gene by parental RNAi reduced fitness in the pea aphid. The results enhance our understanding of the biosynthesis of carotenoid in aphids and provide insights into the potential ecological significance of carotenoids in the adaptation of the aphid's biology to the environment and developing environmentally friendly control strategies for this pest. (Wang) † These authors contributed equally to this work.

Genome‐wide gene expression profiles of the pea aphid (Acyrthosiphon pisum) under cold temperatures provide insights into body color variation

“…Carotenoid pigments synthesizing usually by plants, bacteria, and fungi, are responsible for many red, orange, and yellow colors. The pea aphid endogenously synthesizes carotenoids, unlike other animals, which have several carotenoid‐related genes (such as carotene dehydrogenase: tor ) (Ding et al, 2020; Moran & Jarvik, 2010; Valmalette et al, 2012; Zhang et al, 2018). Mutations causing an amino acid replacement in tor and low‐temperature treatments result in a loss of the red body color in the pea aphid (Moran & Jarvik, 2010).…”

“…The pea aphid synthesizes carotene instead of obtaining it from dietary sources (Moran & Jarvik, 2010; Valmalette et al, 2012). The pea aphid genome encodes abundant enzymes for the various carotenoids synthesis, and these enzymes ultimately contribute to the color polymorphism (Ding et al, 2020; Moran & Jarvik, 2010). Nine genes identified in the pea aphid genome have been associated with carotenoid biosynthesis and related metabolic pathways and are obtained through horizontal gene transfer from fungi (Ding et al, 2020; Moran & Jarvik, 2010; Valmalette et al, 2012; Zhang et al, 2018).…”

“…The pea aphid genome encodes abundant enzymes for the various carotenoids synthesis, and these enzymes ultimately contribute to the color polymorphism (Ding et al, 2020; Moran & Jarvik, 2010). Nine genes identified in the pea aphid genome have been associated with carotenoid biosynthesis and related metabolic pathways and are obtained through horizontal gene transfer from fungi (Ding et al, 2020; Moran & Jarvik, 2010; Valmalette et al, 2012; Zhang et al, 2018). These nine genes can be divided into two categories: five carotenoid synthase/cyclase genes (LOC100161104, LOC100574964, LOC100571777, LOC103308018, and LOC100159332) and four carotenoid desaturase genes (LOC100159050, tor , LOC100169110, and LOC100161380) (Ding et al, 2020; Moran & Jarvik, 2010; Zhang et al, 2018).…”

“…Nine genes identified in the pea aphid genome have been associated with carotenoid biosynthesis and related metabolic pathways and are obtained through horizontal gene transfer from fungi (Ding et al, 2020; Moran & Jarvik, 2010; Valmalette et al, 2012; Zhang et al, 2018). These nine genes can be divided into two categories: five carotenoid synthase/cyclase genes (LOC100161104, LOC100574964, LOC100571777, LOC103308018, and LOC100159332) and four carotenoid desaturase genes (LOC100159050, tor , LOC100169110, and LOC100161380) (Ding et al, 2020; Moran & Jarvik, 2010; Zhang et al, 2018). In the pea aphid, only red individuals have a single carotenoid desaturase ( tor ), and mutation results in a loss of the red color (Moran & Jarvik, 2010).…”

“…In the pea aphid, only red individuals have a single carotenoid desaturase ( tor ), and mutation results in a loss of the red color (Moran & Jarvik, 2010). The parental gene silencing of a carotenoid desaturase gene ( tor ) results in a lower body color intensity in treated aphids and in following generations in vivo (Ding et al, 2020).…”