CIRCADIAN CLOCK-ASSOCIATED1 (CCA1), a well-known central circadian clock regulator, coordinates plant responses to environmental challenges. Its daily rhythmic expression in Arabidopsis thaliana confers host resistance to a caterpillar Trichoplusia ni. However, it is unclear whether CCA1 plays a role in defense against phloem sap-feeding aphids. In this study, we showed that green peach aphid (Myzus persicae) displayed an intrinsic circadian feeding rhythm. Under constant light, wild-type Col-0 co-entrained with aphids in the same light/dark cycles exhibited greater antixenotic activity than plants pre-entrained in the opposite cycle from the aphids. Consistently, circadian mutants cca1-1, cca1-11, lhy-21, ztl-1, ztl-4 and lux-2 suffered more severe damage than wild-type plants when infested by aphids, suggesting a defensive role of the Arabidopsis circadian clock. However, the arrhythmic CCA1-overexpression line (CCA1-OX) displayed strong antixenotic and antibiotic activities despite the loss of circadian regulation. Aphids on CCA1-OX exhibited lower reproduction and smaller body size and weight than those on Col-0. Apparently, CCA1 regulates both clock-dependent and -independent defenses. Systematic investigation based on bioinformatic analyses indicated that the anti-aphid activity conferred by CCA1-OX was due substantially to heightened basal indole glucosinolate levels. Interestingly, aphid feeding induced alternatively spliced intron-retaining CCA1a/b transcripts, normally expressed at low levels, whereas expression of the major fully spliced CCA1 transcript remained largely unchanged. Such post-transcriptional modulation upon aphid infestation presumably can maximize the potential of circadian-mediated defense and stress tolerance while ensuring normal plant development.
