The intricate interplay between cellular circadian rhythms,primarily manifested in the chloroplast redox oscillations-characterized by diel hyperoxidation/reduction cycles of 2-Cys peroxiredoxins-and the nuclear trans...The intricate interplay between cellular circadian rhythms,primarily manifested in the chloroplast redox oscillations-characterized by diel hyperoxidation/reduction cycles of 2-Cys peroxiredoxins-and the nuclear transcription/translation feedback loop(TTFL)machinery within plant cells,demonstrates a remarkable temporal coherence.However,the molecular mechanisms underlying the integration of these circadian rhythms remain elusive.In this study,we reveal that the chloroplast redox protein,NADPH-dependent thioredoxin reductase type C(NTRC),modulates the integration of the chloroplast redox rhythms and nuclear circadian clocks by regulating intracellular levels of reactive oxygen species and sucrose.In NTRC-deficient ntrc mutants,the perturbed temporal dynamics of cytosolic metabolite pools substantially attenuate the amplitude of CIRCADIAN CLOCK ASSOCIATED 1(CCA1)mRNA oscillation while maintaining its inherent periodicity.In contrast,these fluctuations extend the period and greatly reduced the amplitude of GIGANTEA(GI).In alignment with its regulatory role,the chloroplast redox rhythm and TTFL-driven nuclear oscillators are severely disrupted in ntrc plants.The impairements are rescued by NTRC expression but not by the expression of catalytically inactive NTRC(C/S)mutant,indicating that NTRC’s redox activity is essential for synchronizing intracellular circadian rhythms.In return,the canonical nuclear clock component,TIMING OF CAB EXPRESSION 1(TOC1),regulates the diel chloroplast redox rhythm by controlling NTRC expression,as evidenced by the redox cycle of chloroplast 2-Cys peroxiredoxins.This reciprocal regulation suggests a tight coupling between chloroplast redox rhythms and nuclear oscillators.Collectively,our study has identified NTRC as a key circadian modulator,elucidating the intricate connection between the metabolite-dependent chloroplast redox rhythm and the temporal dynamics of nuclear canonical clocks.展开更多
基金supported by the National Research Foundation of Korea(NRF)grants funded by the MSIT(grant nos.2021R1A2C1093478 and 2022R1A5A1031361 to S.Y.L.)by the Basic Science Research Program of NRF funded by the Ministry of Education(RS-2024-00462888 to S.K.P.+1 种基金NRF-2022R111A1A01065660 to H.B.C.RS-2023-00250106 to S.D.W.).
文摘The intricate interplay between cellular circadian rhythms,primarily manifested in the chloroplast redox oscillations-characterized by diel hyperoxidation/reduction cycles of 2-Cys peroxiredoxins-and the nuclear transcription/translation feedback loop(TTFL)machinery within plant cells,demonstrates a remarkable temporal coherence.However,the molecular mechanisms underlying the integration of these circadian rhythms remain elusive.In this study,we reveal that the chloroplast redox protein,NADPH-dependent thioredoxin reductase type C(NTRC),modulates the integration of the chloroplast redox rhythms and nuclear circadian clocks by regulating intracellular levels of reactive oxygen species and sucrose.In NTRC-deficient ntrc mutants,the perturbed temporal dynamics of cytosolic metabolite pools substantially attenuate the amplitude of CIRCADIAN CLOCK ASSOCIATED 1(CCA1)mRNA oscillation while maintaining its inherent periodicity.In contrast,these fluctuations extend the period and greatly reduced the amplitude of GIGANTEA(GI).In alignment with its regulatory role,the chloroplast redox rhythm and TTFL-driven nuclear oscillators are severely disrupted in ntrc plants.The impairements are rescued by NTRC expression but not by the expression of catalytically inactive NTRC(C/S)mutant,indicating that NTRC’s redox activity is essential for synchronizing intracellular circadian rhythms.In return,the canonical nuclear clock component,TIMING OF CAB EXPRESSION 1(TOC1),regulates the diel chloroplast redox rhythm by controlling NTRC expression,as evidenced by the redox cycle of chloroplast 2-Cys peroxiredoxins.This reciprocal regulation suggests a tight coupling between chloroplast redox rhythms and nuclear oscillators.Collectively,our study has identified NTRC as a key circadian modulator,elucidating the intricate connection between the metabolite-dependent chloroplast redox rhythm and the temporal dynamics of nuclear canonical clocks.
