Comparative transcriptional analysis and identification of hub genes associated with wing differentiation of male in Aphis gossypii

Abstract

Background Aphis gossypii Glover (Hemiptera: Aphididae), a worldwide polyphagous phloem-feeding agricultural pest, has three wing morphs (winged parthenogenetic female, gynopara and male) in the life cycle, in which the exclusive males could fly from second hosts to winter hosts and are essential for gene exchange of cotton aphid populations from different host or regions. However, the molecular mechanism of wing differentiation of male in A. gossypii remains unclear. Results Morphological observation of male A. gossypii showed that no distinct differences existed in the external morphologies of the 1st and 2nd instar nymphs, while the obvious differentiation of wing buds started in 3rd instar nymphs and were visible via naked eyes in 4th instar nymphal stage, then adult male emerged with fully wings. According to morphological dynamic changes, the development of wings in males were divided into four stages: preliminary stage (1st instar to 2nd instar), prophase (3rd instar), metaphase (4th instar), anaphase (5th instar). Results of feeding behavior monitoring via EPG (electrical penetration graph) technology indicated that although the male cotton aphids had strong desire to feed (longer duration of C 55.24%, F 5.05% and Pd waves 2.56%), its feeding efficiency to summer host cotton was low (shorter E1 3.56% and E2 waves 2.63%). Dynamic transcriptome analysis of male aphid at 5 different developmental periods found that in 3rd instar nymphs, the number of up-regulated DEGs were significant increased, and time-course gene transcriptional pattern analyses results also showed numerous genes categorized in clusters 3, 5, and 8 had the highest expressed level, which were consistent with morphological changes of wing buds. These results indicate that the 3rd instar nymphs are the critical stage of wing bud differentiation in males. Further, pathway enrichment analysis of DEGs and WGCNA analysis revealed that the neuroactive ligand-receptor interaction, Ras signaling pathway, dopaminergic synapse, circadian entrainment and corresponding the candidate hub genes PLK1, BUB1, SMC2, TUBG, ASPM, the kinesin family members (KIF23, KIF20, KIF18-19) and the novel subfamily of serine/threonine (Aurora kinase A and Aurora kinase B) probably played important roles in the critical stage of wing bud differentiation. Conclusion This study explored changes of the morphological and transcriptional level from the 1st instar nymphs to adults of male cotton aphid, revealed the phenomenon of low feeding efficiency of winged male cotton aphid on secondary hosts, and identified key signaling pathways and potential hub genes potentially involved in wing bud differentiation of male in A. gossypii.