CIRCADIAN CLOCK-ASSOCIATED1 Controls Resistance to Aphids by Altering Indole Glucosinolate Production

Abstract

CIRCADIAN CLOCK-ASSOCIATED1 (CCA1), a well-known central circadian clock regulator, coordinates plant responses to environmental challenges. Its daily rhythmic expression in Arabidopsis (<i>Arabidopsis thaliana</i>) confers host resistance to the caterpillar <i>Trichoplusia ni</i> 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 (<i>Myzus persicae</i>) displayed an intrinsic circadian feeding rhythm. Under constant light, wild-type Columbia-0 (Col-0) Arabidopsis plants coentrained with aphids in the same light/dark cycles exhibited greater antixenotic activity than plants preentrained in the opposite cycle from the aphids. Consistently, circadian mutants <i>cca1-1</i>, <i>cca1-11</i>, <i>lhy-21</i>, <i>ztl-1</i>, <i>ztl-4</i>, and <i>lux-2</i> suffered more severe damage than Col-0 plants when infested by aphids, suggesting that the Arabidopsis circadian clock plays a defensive role. However, the arrhythmic <i>CCA1</i> overexpression line (<i>CCA1-OX</i>) displayed strong antixenotic and antibiotic activities despite its loss of circadian regulation. Aphids feeding on <i>CCA1-OX</i> plants exhibited lower reproduction and smaller body size and weight than those on Col-0. Apparently, CCA1 regulates both clock-dependent and -independent defense responses. Systematic investigation based on bioinformatics analyses indicated that resistance to aphids in <i>CCA1-OX</i> plants was due primarily to heightened basal indole glucosinolate levels. Interestingly, aphid feeding induced alternatively spliced intron-retaining <i>CCA1a/b</i> transcripts, which are normally expressed at low levels, whereas expression of the major fully spliced <i>CCA1</i> transcript remained largely unchanged. We hypothesize that posttranscriptional modulation of <i>CCA1</i> expression upon aphid infestation maximizes the potential of circadian-mediated defense and stress tolerance while ensuring normal plant development.