A sucrose feed-back loop promotes sucrose accumulation in cotyledons to facilitate sugar-ethylene signaling mediated-greening of arabidopsis seedlings

Xiao Ying Cao, Chen Tong, Xin Rong Mu, Qin-Xin Bao, Li Na Xue, Wei-Ying Meng, Yue Fei, Chang Yue Liu, Gary J. Loake, Ji-Hong Jiang, Lai-Sheng Meng

Research output: Contribution to journalArticlepeer-review

Abstract

The switch from skoto-to-photomorphogenesis is indispensable for seedling survival and development. Integral to this process is etiolated seedling greening, where the onset of illumination initiates an etioplast-to-chloroplast transition. While sugars have long been shown to affect etiolated seedling greening, the underpinning molecular mechanism(s) have remained elusive. Further, whereas the mechanical stress of the soil has been reported to activate ethylene production to promote cotyledon greening by a key ethylene component ETHYLENE-INSENSITIVE3 (EIN3) controlling a few phytochrome and associated factors, how the mechanical stress of the soil induces ethylene production remains unclear. Here we demonstrate that cotyledon greening of etiolated seedlings is induced preferentially by sucrose relative to other sugars. We further identify a sucrose feed-back loop. In details, under darkness, sucrose in germinating seeds preferentially induces expression of 1-amino-cyclopropane-1-carboxylate synthase (ACS7), encoding a key enzyme involved in ethylene biosynthesis. Induced ethylene activates EIN3 by its canonical signal transduction pathway. Activated EIN3 directly inhibits the function of sucrose transporter 2 (SUC2, a major transporter of sucrose phloem loading) to block sucrose export from cotyledons and thereby elevate sucrose accumulation in cotyledons. Therefore, under darkness, the sucrose feed-back loop (Sucrose-ACS7-ethylene-EIN3-SUC2-Sucrose) continually promotes sucrose accumulation by inhibiting sucrose export from cotyledons. Further, following white light illumination, accumulated sucrose activates EIN3 by the sucrose feed-back loop. Activated EIN3 directly suppresses the function of phytochrome A (PHYA, a far-red light photoreceptor and an inhibitor of etiolated seedling greening), to promote cotyledon greening. Together, under darkness, the sucrose feed-back loop induces substantial sucrose accumulation, which in turn induces ethylene production and activates EIN3, to control a few phytochrome and associated factors, including PHYA, to trigger etiolated seedling greening in the onset of illumination. Therefore, the sucrose feed-back loop induced- sucrose accumulation is a prerequisite for sucrose-/ethylene signaling mediated-etiolated seedling greening. We therefore posit that the sucrose feed-back loop induced- sucrose accumulation following seed germination facilitates a developmental switch in seedlings from skoto-to-photomorphogenesis.
Original languageEnglish
JournalCell Reports
Publication statusAccepted/In press - 13 Dec 2021

Keywords

  • cotyledon greening
  • ethylene-insensitive3 (ein3)
  • phytochrome a (phya)
  • ethylene
  • sucrose transporter 2 (suc2)
  • sucrose phloem loading

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