Abstract

Leaf senescence is the terminal stage of leaf development. Both light and the plant hormone ethylene play important roles in regulating leaf senescence. However, how they coordinately regulate leaf senescence during leaf development remains largely unclear. In this study, we show that FHY3 and FAR1, two homologous proteins essential for phytochrome A-mediated light signaling, physically interact with and repress the DNA binding activity of EIN3 (a key transcription factor essential for ethylene signaling) and PIF5 (a bHLH transcription factor negatively regulating light signaling), and interfere with their DNA binding to the promoter of ORE1, which encodes a key NAC transcription factor promoting leaf senescence. In addition, we show that FHY3, PIF5, and EIN3 form a tri-protein complex(es) and that they coordinately regulate the progression of leaf senescence. We show that during aging or under dark conditions, accumulation of FHY3 protein decreases, thus lifting its repression on DNA binding of EIN3 and PIF5, leading to the increase of ORE1 expression and onset of leaf senescence. Our combined results suggest that FHY3 and FAR1 act in an age gating mechanism to prevent precocious leaf senescence by integrating light and ethylene signaling with developmental aging.

Highlights

  • Leaf senescence is the last stage of leaf development, during which macromolecules are degraded in an orderly fashion, and the resulting nutrients are mobilized from old leaves to actively growing tissues or storage organs, increasing plant fitness (Lim et al, 2007)

  • We previously showed that FHY3 and FAR1 proteins physically interact with both EIN3 and PIF5 transcription factors (Liu et al, 2017, 2020), while both EIN3 and PIF5 were reported to up-regulate the expression of ORE1, a key NAC transcription factor promoting leaf senescence (Sakuraba et al, 2014; Qiu et al, 2015)

  • We found that the detached leaves from fhy3 far1 mutants showed significantly faster senescence than the wild type, with significantly lower chlorophyll content (Figures 1A,B), consistent with their effects on age-dependent senescence

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Summary

Introduction

Leaf senescence is the last stage of leaf development, during which macromolecules (such as nucleic acids and proteins) are degraded in an orderly fashion, and the resulting nutrients are mobilized from old leaves to actively growing tissues or storage organs, increasing plant fitness (Lim et al, 2007). Illuminating, several GRNs of NAC (NAM/ATAF/CUC) and WRKY transcription factors have been shown to change dynamically as leaf senescence progresses (Kim et al, 2016). It has been shown that expression of ORE1 is positively regulated by several transcription factors, including EIN3/EIL1 (ETHYLENE INSENSITIVE 3/EIN3-LIKE 1), ATAF1 (ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR 1), ABI5/EEL (ABA INSENSITIVE 5/ENHANCED EM LEVEL), and PIF4/5 (PHYTOCHROME-INTERACTING FACTOR 4/5) (Li et al, 2013; Sakuraba et al, 2014; Song et al, 2014). ORE1 acts in multiple coherent feedforward loops to promote leaf senescence by integrating signals from ethylene, abscisic acid (ABA), salinity and light/dark into developmental aging

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