Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2

Abstract

The polycomb repressive complex 2 (PRC2) regulates epigenetic gene repression in eukaryotes. Mechanisms controlling its developmental specificity and signal-responsiveness are poorly understood. Here, we identify an oxygen-sensitive N-terminal (N-) degron in the plant PRC2 subunit VERNALIZATION(VRN) 2, a homolog of animal Su(z)12, that promotes its degradation via the N-end rule pathway. We provide evidence that this N-degron arose early during angiosperm evolution via gene duplication and N-terminal truncation, facilitating expansion of PRC2 function in flowering plants. We show that proteolysis via the N-end rule pathway prevents ectopic VRN2 accumulation, and that hypoxia and long-term cold exposure lead to increased VRN2 abundance, which we propose may be due to inhibition of VRN2 turnover via its N-degron. Furthermore, we identify an overlap in the transcriptional responses to hypoxia and prolonged cold, and show that VRN2 promotes tolerance to hypoxia. Our work reveals a mechanism for post-translational regulation of VRN2 stability that could potentially link environmental inputs to the epigenetic control of plant development.

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

“…Since NO was previously shown to control proteolysis of ERFVIIs and other Met 1 -Cys 2 N-degron targets 14,19,27 , we hypothesized that ethylene may regulate NO levels. Roots treated with the NO probe 4-Amino-5-Methylamino-2’,7’-Difluorofluorescein (DAF-FM) Diacetate 28 revealed an ethylene-induced depletion in fluorescence, indicating that ethylene mediates NO levels (Fig.…”

“…The possible existence of undiscovered plant O 2 sensors was recently discussed and could potentially fulfil this role 35 . Furthermore, the current discovery of ethylene-mediated stability of ERFVIIs paves the way towards unravelling how ethylene could influence the function of the other recently discovered PRT6 N-degron pathway targets VERNALIZATION2 (VRN2) and LITTLE ZIPPER2 (ZPR2) 25,27 .…”

Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants

“…It has been reported that plants transduce NO signal through S‐nitrosylation of protein arginine methyl transferase 5 involved in protein methylation machinery and the subsequent epigenetic regulation of pre‐mRNA splicing, DNA damage repair, and mRNA translation (Blanc & Richard, ) in response to environmental alterations (Hu et al, ). It is worth mentioning that the polycomb repressive complex 2 subunit VERNALIZATION 2 is regulated, like ERFVIIs, in an O 2 ‐ and NO‐dependent manner involving the Cys–Arg branch of the N‐end rule proteolytic pathway (Gibbs et al, ), thus representing an additional support for a functional link between NO signaling and epigenetic regulation. This regulatory mechanism is consistent with the reported role for NO as a repressor of the floral transition (He et al, ), as VERNALIZATION 2 promotes the transition from vegetative to reproductive development during vernalization by methylating and silencing the floral repressor gene FLOWERING LOCUS C (Gendall, Levy, Wilson, & Dean, ).…”

“…repressive complex 2 subunit VERNALIZATION 2 is regulated, like ERFVIIs, in an O 2and NO-dependent manner involving the Cys-Arg branch of the N-end rule proteolytic pathway(Gibbs et al, 2018), thus representing an additional support for a functional link between NO signaling and epigenetic regulation. This regulatory mechanism is consistent with the reported role for NO as a repressor of the floral transition(He et al, 2004), as VERNALIZATION 2 promotes theFIGURE 3 NO sensing based on the N-end rule pathway degradation of ERFVII transcription factors.…”

Differential N-end rule degradation of RIN4/NOI fragments generated by the AvrRpt2 effector protease

“…1B). The plant Arg/N-degron pathway has been shown to regulate various developmental and physiological processes in Arabidopsis (Graciet et al, 2009;Holman et al, 2009;Abbas et al, 2015;Gibbs et al, 2018;Zhang et al, 2018) and in barley (Mendiondo et al, 2016;Vicente et al, 2017), as well as gametophytic development in the moss Physcomitrella patens (Schuessele et al, 2016). Furthermore, protein degradation via this pathway plays a key role in the control of flooding tolerance (Gibbs et al, 2011;Licausi et al, 2011).…”