The PRT6 N‐degron pathway restricts VERNALIZATION 2 to endogenous hypoxic niches to modulate plant development

Abstract

VERNALIZATION2 (VRN2), an angiosperm-specific subunit of the polycomb repressive complex 2 (PRC2), is an oxygen (O 2 )-regulated target of the PCO branch of the PRT6 N-degron pathway of ubiquitin-mediated proteolysis. How this post-translational regulation coordinates VRN2 activity remains to be fully established.Here we use Arabidopsis thaliana ecotypes, mutants and transgenic lines to determine how control of VRN2 stability contributes to its functions during plant development.VRN2 localizes to endogenous hypoxic regions in aerial and root tissues. In the shoot apex, VRN2 differentially modulates flowering time dependent on photoperiod, whilst its presence in lateral root primordia and the root apical meristem negatively regulates root system architecture. Ectopic accumulation of VRN2 does not enhance its effects on flowering, but does potentiate its repressive effects on root growth. In late-flowering vernalization-dependent ecotypes, VRN2 is only active outside meristems when its proteolysis is inhibited in response to cold exposure, as its function requires concomitant cold-triggered increases in other PRC2 subunits and cofactors.We conclude that the O 2 -sensitive N-degron of VRN2 has a dual function, confining VRN2 to meristems and primordia, where it has specific developmental roles, whilst also permitting broad accumulation outside of meristems in response to environmental cues, leading to other functions.

Conserved and Opposite Transcriptome Patterns during Germination in Hordeum vulgare and Arabidopsis thaliana

“…It was notable that a group of 22 AP2/EREPB TFs displayed upregulation in abundance at the earliest stages of germination (3 to 12 h) and downregulation in transcript abundance at the later stages of abundance (24 to 48 h) in barley ( Figure 7 D), as well as the fact that AP2 TFs are associated with responses to hypoxia [ 64 ]. It has been shown for both root and shoot meristems that hypoxia plays an important role in development, with the N-end rule determining the stability of TFs to activate a hypoxic response [ 65 ]. The upregulation of AP2 factors at the start of germination may indicate that the larger barley grain is under hypoxic conditions after imbibition and at the earliest stages of germination.…”

Acquisition of hypoxia inducibility by oxygen sensing N-terminal cysteine oxidase in spermatophytes

“…However, oxidation of ZPR2 by PCO has not been tested yet. All these transcriptional regulators regulate adaptive responses to ambient and internal oxygen fluctuations (Giuntoli et al, 2017, Weits et al, 2020, Labandera et al, 2020). Recently, a PCO-counterpart of metazoans, the Cysteamine Dioxygenase ADO, was also found to regulate stability of Methionine-Cysteine initiating proteins (Masson et al 2019).…”

Nitric oxide function during oxygen deprivation in physiological and stress processes

“…ERFVII group was the first substrate of the PCO branch of the PRT6 N-degron pathway described in plants ( Gibbs et al , 2011 ; Licausi et al , 2011 ) followed by the transcriptional regulators polycomb repressive complex 2 subunit VERNALIZATION 2 (VRN2) ( Gibbs et al , 2018 ) and LITTLE ZIPPER 2 (ZPR2) ( Weits et al , 2019 ). N-degron pathway substrates regulate important aspects of plant development such as seed storage mobilization ( Zhang et al ., 2018 a , b ), germination ( Holman et al , 2009 ; Gibbs et al , 2014 ), photomorphogenesis ( Abbas et al , 2015 ), stomatal closure ( Gibbs et al , 2014 ), shoot and leaf development ( Graciet et al , 2009 ), root architecture ( Shukla et al , 2019 ), SAM function ( Weits et al , 2019 ), vernalization ( Gibbs et al , 2018 ; Labandera et al , 2020 ), flowering ( Vicente et al , 2017 ), or leaf senescence ( Yoshida et al , 2002 ), and also regulates stress responses such as flooding ( Hartman et al , 2019 ) or pathogen attack ( de Marchi et al , 2016 ; Vicente et al , 2019 ; Till et al , 2019 ).…”

“…In the case of VRN2 and ZPR2, these transcriptional regulators are located in hypoxic niches. ZPR2 is found in the SAM where it controls the meristem maintenance; VRN2, besides the SAM, is also located in young leaf primordia and root meristematic zones, and has a role in vernalization and root architecture ( Weits et al , 2019 ; Labandera et al , 2020 ). The physiological hypoxia that exists in these zones prevents these proteins from degradation through the N-degron pathway.…”

“…Some substrates of the N-degron pathway are found in meristems, where they have important functions ( Gibbs et al , 2018 ; Weits et al , 2019 ; Labandera et al , 2020 ). The physiological hypoxia that exists in the meristems prevents its degradation through the N-degron pathway.…”