Seasonal photoperiodism regulates the expression of cuticular and signalling protein genes in the pea aphid (original) (raw)
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Transcriptomic and proteomic analyses of seasonal photoperiodism in the pea aphid
BMC genomics, 2009
Background: Aphid adaptation to harsh winter conditions is illustrated by an alternation of their reproductive mode. Aphids detect photoperiod shortening by sensing the length of the night and switch from viviparous parthenogenesis in spring and summer, to oviparous sexual reproduction in autumn. The photoperiodic signal is transduced from the head to the reproductive tract to change the fate of the future oocytes from mitotic diploid embryogenesis to haploid formation of gametes. This process takes place in three consecutive generations due to viviparous parthenogenesis. To understand the molecular basis of the switch in the reproductive mode, transcriptomic and proteomic approaches were used to detect significantly regulated transcripts and polypeptides in the heads of the pea aphid Acyrthosiphon pisum.
Cuticular proteins and seasonal photoperiodism in aphids
Insect Biochemistry and Molecular Biology, 2010
For poikilotherm animals such as insects, extreme temperatures can be a severe issue in continental regions. Aphids, which reproduce in spring and summer by viviparity, are prone to death in hard winter conditions. These species exhibit reproductive plasticity adapted to winter by producing oviparous females in autumn, which lay overwintering eggs. This switch is driven by photoperiodism, and long nights are sufficient to trigger the change in reproductive mode. Global transcriptomic analyses applied to the pea aphid Acyrthosiphon pisum for which genomic resources are now available have allowed the identification of several genetic programs regulated by photoperiod shortening. Unexpectedly, one of these genetic programs concerns cuticle proteins and cuticle structure. This opens new tracks for investigations and poses new hypotheses on the link between cuticle modification and neuronal signalisation of photoperiod in aphids in response to seasonal photoperiodism. This review focuses on the description of cuticular protein genes in the pea aphid and their regulation during the change of reproductive mode.
Identification of a gene overexpressed in aphids reared under short photoperiod
Insect Biochemistry and Molecular Biology, 2003
Most aphids develop a cyclic parthenogenesis life-cycle. After several generations of viviparously produced parthenogenetic females, follows a single annual generation of sexual individuals, usually in autumn, that mate and lay the sexual eggs. Shortening of photoperiod at the end of the summer (together with temperature) is a key factor inducing the sexual response. Currently no genes involved in the cascade of events that lead to the appearance of sexual forms have been reported. After a Differential Display RT-PCR survey performed on Acyrthosiphon pisum aphids, we identified a gene that is overexpressed in aphids reared under short photoperiod conditions that induce sexuality in this species. This cDNA (called ApSDI-1) shows similarities with a protein involved in amino acid transport in GABAergic neurons. Since several studies implicate GABAergic transmission in the generation and modulation of circadian rhythmicity, we propose that ApSDI-1 could be involved in the transduction of the photoperiodic message and therefore be a candidate to participate at some point in processes that trigger the sexual response in aphids. This is the first gene identified in aphids whose expression is governed by the photoperiod.
Insect Molecular Biology, 2010
The molecular basis of circadian clocks is highly evolutionarily conserved and has been best characterized in Drosophila and mouse. Analysis of the Acyrthosiphon pisum genome revealed the presence of orthologs of the following genes constituting the core of the circadian clock in Drosophila: period (per), timeless (tim), Clock, cycle, vrille, and Pdp1. However, the presence in A. pisum of orthologs of a mammal-type in addition to a Drosophila-type cryptochrome places the putative aphid clockwork closer to the ancestral insect system than to the Drosophila one. Most notably, five of these putative aphid core clock genes are highly divergent and exhibit accelerated rates of change (especially per and tim orthologs) suggesting that the aphid circadian clock has evolved to adapt to (unknown) aphid-specific needs. Additionally, with the exception of jetlag (absent in the aphid) other genes included in the Drosophila circadian clock repertoire were found to be conserved in A. pisum. Expression analysis revealed circadian rhythmicity for some core genes as well as a significant effect of photoperiod in the amplitude of oscillations.
Insect Molecular Biology, 2011
Most aphids show reproductive polyphenism, i.e. they alternate their reproductive modes from parthenogenesis to sexual reproduction in response to short photoperiod. Although juvenile hormone (JH) has been considered a likely candidate for regulating the transition from asexual to sexual reproduction after photoperiod sensing, there are few studies investigating the direct relationship between JH titers and the reproductive mode change. In addition, the sequencing of the pea aphid genome now allows identification of the genes involved in the JH pathway which then allows us to examine their expression levels in relation to the reproductive-mode switch. Using LC-MS in the pea aphid, JHIII titer was shown to be lower in aphids producing sexual morphs under short-days than in aphids producing parthenogenetic morphs in long-days. The expression levels of genes upstream and downstream of JH action were quantified by real-time qRT-PCR across the reproductive mode change. The expression level of JH esterase (JHE), which is responsible for JH degradation, was significantly higher in aphids reared under short-days. This suggests that the up-regulation of the JH degradation pathway may be responsible for the lower JHIII titer in aphids exposed to short-days, leading to the production of sexual morphs.
Deciphering reproductive polyphenism in aphids
Invertebrate Reproduction & Development, 2005
Polyphenism, which allows one given genotype to produce several discrete phenotypes, is an extreme case of phenotypic plasticity and is mainly found in arthropods. Social insects are the canonical example of polyphenism with the development of castes in the colonies. However, aphids display one of the largest range of polyphenisms, notably by producing winged or wingless, as well as asexual or sexual forms, depending on environmental conditions. During spring and summer, aphids reproduce by viviparous parthenogenesis, whereas in autumn they enter sexual reproduction. This switch in reproductive mode is triggered by changes in photoperiod and temperature. Here, the data accumulated since the 1960s on the identification of photoperiodic clocks, counter and putative neural photoreceptors that participate in this reproductive shift are reviewed. After perception, the photoperiodic signal is transduced through the secretion of hormones (juvenile hormones may well be involved) which, in turn, may act on the target cells, namely the oocytes. In short-day conditions, oocytes enter meiosis and produce haploid eggs which develop a 2n embryo after fertilisation. By contrast, in long-day conditions, a single maturation division produces 2n oocytes which immediately enter parthenogenetic embryogenesis. A physiological model of the determination of sexual vs. asexual reproduction in aphids is proposed and viewed from the perspective of newly initiated molecular studies.
European Journal of Entomology, 2003
Wild females of Pyrrhocoris apterus exhibit seasonal changes in neuroendocrine activity and, consequently, reproduction. Long days (18 h light/6 h dark) (LD) stimulate reproduction, whereas short days (12 h light/12 h dark) (SD) induce reproductive arrest (diapause). This study reveals how photoperiod influences the expression of the circadian clock gene, period (per) in the insect's head. There is only a weak diurnal rhythm inper mRNA expression under LD and SD. However, levels of per mRNA are consistently higher (up to 10-fold) under SD than under LD. The influence of photoperiod on per gene expression is linked to a developmental output (diapause vs. reproduction); mutant females, reproducing under both LD and SD, show lowper mRNA levels under both photoperiodic conditions. Thus, the magnitude of per gene expression may be important to the translation of photoperi odic signals into a hormonal message. Levels of per mRNA are related to properties of locomotor activity rhythms. Lowper mRNA levels (displayed by wild females in LD and mutant females in both LD and SD) are associated with long free-running periods (t~26-27 h) and late peaks of activity (yR >L10-12 h), whereas high per mRNA levels coincide with short free-running periods (t~24 h) and early peaks of activity (yR >L4-6 h). Overall, the data provide a background for a molecular approach to the long standing question about the role of the circadian system in insect photoperiodism.
Insect Molecular Biology, 2010
Aphids exhibit unique attributes, such as polyphenisms and specialized cells to house endosymbionts, that make them an interesting system for studies at the interface of ecology, evolution and development. Here we present a comprehensive characterization of the developmental genes in the pea aphid, Acyrthosiphon pisum, and compare our results to other sequenced insects. We investigated genes involved in fundamental developmental processes such as establishment of the body plan and organogenesis, focusing on transcription factors and components of signalling pathways. We found that most developmental genes were well conserved in the pea aphid, although many lineage-specific gene duplications and gene losses have occurred in several gene families. In particular, genetic components of transforming growth factor beta (TGFb) Wnt, JAK/STAT (Janus kinase/signal transducer and activator of transcription) and EGF (Epidermal Growth Factor) pathways appear to have been significantly modified in the pea aphid.
Archives of Insect Biochemistry and Physiology, 2016
To obtain clues to the link between the molecular mechanism of circadian and photoperiod clocks, we cloned two circadian clock genes, period (per) and timeless (tim) from the moth Sesamia nonagrioides, which undergoes facultative diapause controlled by photoperiod. Sequence analysis revealed a high degree of conservation among the compared insects fοr both genes. We also investigated the expression patterns of per and tim in brains of larvae growing under 16L:8D (long days), constant darkness (DD) and 10L:14D (short days) conditions by qPCR assays. The results showed that mRNA accumulations encoding both genes exhibited diel oscillations under different photoperiods. The oscillation of per and tim mRNA, under short-day photoperiod differed from long-day. The difference between longday and short-day conditions in the pattern of mRNA levels of per and tim appears to distinguish photoperiodic conditions clearly and both genes were influenced by photoperiod in different ways. We infer that not all photoperiodic clocks of insects interact with circadian clocks in the same fashion. Our results suggest that transcriptional regulations of the both clock genes act in the diapause programing in S. nonagrioides. The expression patterns of these genes are affected by photoperiod but runs with 24 h by entrainment to daily environmental cues.
PLoS ONE, 2011
Piwi-interacting RNAs (piRNAs) are known to regulate transposon activity in germ cells of several animal models that propagate sexually. However, the role of piRNAs during asexual reproduction remains almost unknown. Aphids that can alternate sexual and asexual reproduction cycles in response to seasonal changes of photoperiod provide a unique opportunity to study piRNAs and the piRNA pathway in both reproductive modes. Taking advantage of the recently sequenced genome of the pea aphid Acyrthosiphon pisum, we found an unusually large lineage-specific expansion of genes encoding the Piwi sub-clade of Argonaute proteins. In situ hybridisation showed differential expressions between the duplicated piwi copies: while Api-piwi2 and Api-piwi6 are ''specialised'' in germ cells their most closely related copy, respectively Api-piwi5 and Api-piwi3, are expressed in the somatic cells. The differential expression was also identified in duplicated ago3: Api-ago3a in germ cells and Api-ago3b in somatic cells. Moreover, analyses of expression profiles of the expanded piwi and ago3 genes by semi-quantitative RT-PCR showed that expressions varied according to the reproductive types. These specific expression patterns suggest that expanded aphid piwi and ago3 genes have distinct roles in asexual and sexual reproduction.