Seasonal photoperiodism regulates the expression of cuticular and signalling protein genes in the pea aphid
Introduction
Alternation of day and night and their length variation across seasons in temperate regions are detected by most organisms and commonly used as a reliable signal to anticipate environmental changes. Plants and animals respond to these photoperiodic changes often through spectacular physiological and developmental modifications leading to phenotypes more suitable for future environmental conditions (Gwinner, 2003; Searle and Coupland, 2004). Winter is by far the most difficult testing period in the life cycle of many organisms, especially for cold-blooded animals like insects. As an example, diapause is a mechanism frequently used by insects to deal with adverse seasonal conditions and entering into diapause usually relies on photoperiodic cues sensed by insects (Tauber and Kyriacou, 2001). The molecular mechanisms involved in the detection and transduction of seasonal photoperiodism in insects are however still poorly described (Danks, 2003; Saunders, 2005).
In aphids, seasonal photoperiodism induces dramatic modifications of their reproductive mode. While aphid populations spend spring and summer by performing fast parthenogenetic (clonal) multiplication, when winter is approaching, they can produce sexual forms that mate and lay cold-resistant and diapausing eggs (Tagu et al., 2005). This switch from clonal to sexual reproduction is mainly triggered by day length and compensated by temperature. Aphid head is the centre for the perception of photoperiodic cues and this signal is thought to be directly sensed by the head capsule—not the eyes—through the cuticle and probably by the brain (Lees, 1964; Steel and Lees, 1977). A group of neurosecretory cells located near the protocerebrum in the brain of the aphid Megourae viciae has been shown to be part of the cellular effectors of the photoperiodic response (Steel and Lees, 1977). The putative photoperiodic receptors have been localized close to these cells by immunocytochemical techniques (Gao et al., 1999). The transduction of the signal probably involves endocrine glands, like corpora allata located in the head that produce and secrete juvenile hormone (JH), known to control several developmental processes in insects. The production of sexual aphids can be inhibited by treatment with ectopic JH, indicating that this hormone could be one of the putative molecular effectors of the photoperiodic response (Hardie, 1981). However, the transduction of the photoperiodic signal is complicated by the so-called telescoping of generations in aphids, since clonal progenies also containing future embryos of the next generation develop inside the abdomen of these insects. The grand mother is the first individual exposed to short days, but sexual morphs will be the grand children. Thus, the photoperiodic signal sensed by the adult has to be transduced not only from the brain to the ovariole of one generation, but across generations. So far, only one study attempted to analyse the influence of seasonal photoperiodism on the level of expression of aphid genes. This work identified a protein involved in the transport of amino acids in GABAergic neurons (Ramos et al., 2003).
Our goal was to detect a broader array of genes specifically regulated by day-length shortening in the pea aphid, Acyrthosiphon pisum, through carefully controlled biological experiments. The head transcriptome was chosen in order to target the first steps of the photoperiodic response, which possibly take place into the brain and nearby nervous structures. Using cDNA microarrays and quantitative RT-PCR, we identified cuticular and signalling protein genes expressed in heads of the pea aphid across two generations: their role in the regulation of seasonal photoperiodism is discussed.
Section snippets
Materials and methods
All the microarray data and procedures have been deposited in the Gene Expression Omnibus database under the series accession number GSE6363.
Production of sexual morphs in YR2 clone of the pea aphid
Production of sexual morphs in aphids requires several consecutive days of short photoperiod. In order to precisely characterize the photoperiodic response of the tested clone YR2, individuals were reared under short photoperiod for 5, 6, 7, 8, 9 or 10 days, before being shifted to long photoperiod (Fig. 2). Progeny of each aphid was then recorded for each number of consecutive SD. For aphids reared from 5 to 9 days at SD, both parthenogenetic females and males were produced but no sexual
Conclusion
This first large transcriptomic analysis of seasonal photoperiodism in aphids gives evidence from both microarray and Q-RT-PCR data of the regulation of several structural and signalling protein genes all along the process of sexual morph production by parthenogenetic individuals. The role of these candidate genes in the regulation of aphid photoperiodism needs to be confirmed and precised by deeper studies. These should include a careful examination of their spatial regulation across different
Acknowledgements
The authors would like to thank A. Monnier and S. Mottier from the OUEST-Genopole transcriptomic facilities (UMR 6061, University of Rennes), and A. Le Cam from INRA-SCRIBE transcriptomic facilities (IFR 140 GFAS, Rennes) the INRA and Agenae transcriptomic platform (INRA Scribe, Rennes). F. Legeai (URGI, INRA Evry) and J.P. Gauthier (UMR BiO3P, Rennes) are acknowledged for bioinformatic expertise. Prof. J. Hardie (Imperial College, London) and Alain Henaut (CNRS) are thanked for their comments.
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Present address: Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología (PVyB), Unidad de Entomología Carretera de Moncada a Náquera km 4,5, 46113 Moncada Valencia, Spain.