An apical hypoxic niche sets the pace of shoot meristem activity

Weits, Daan A.; Kunkowska, Alicja B; Kamps, Nicholas C. W.; Portz, Katharina; Packbier, Niko K.; Venza, Zoe Nemec; Gaillochet, Christophe; Lohmann, Jan U.; Pedersen, Ole; Dongen, Joost Thomas van; Licausi, Francesco

doi:10.1038/s41586-019-1203-6

Cited by 175 publications

(209 citation statements)

References 59 publications

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“…In addition, as both O 2 and NO promote ERFVII proteolysis 17 , and since ethylene was administered at ambient O 2 conditions (21%; normoxia) and did not lead to hypoxia in desiccators (Supplementary Figure 7c), it is unlikely that hypoxia causes the observed ERFVII stabilization. Furthermore, while recent reports show that plants contain a hypoxic niche in shoot apical meristems and lateral root primordia 25,26 , we did not observe enhanced hypoxia target gene expression in root tips exposed ethylene treatments (Supplementary Figure 5), ruling out ethylene-enhanced local hypoxia in these tissues.…”

Section: Resultscontrasting

confidence: 81%

“…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 .…”

Section: Discussionmentioning

confidence: 99%

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

Hartman

Liu

Veen

et al. 2019

Preprint

114

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25 Timely perception of adverse environmental changes is critical for survival. Dynamic 26 changes in gases are important cues for plants to sense environmental perturbations, such 27 as submergence. In Arabidopsis thaliana, changes in oxygen and nitric oxide (NO) control 28 the stability of ERFVII transcription factors. ERFVII proteolysis is regulated by the N-29 degron pathway and mediates adaptation to flooding-induced hypoxia. However, how 30 plants detect and transduce early submergence signals remains elusive. Here we show that 31 plants can rapidly detect submergence through passive ethylene entrapment and use this 32 signal to pre-adapt to impending hypoxia. Ethylene can enhance ERFVII stability prior to 33 hypoxia by increasing the NO-scavenger PHYTOGLOBIN1. This ethylene-mediated NO 34 depletion and consequent ERFVII accumulation pre-adapts plants to survive subsequent 35 hypoxia. Our results reveal the biological link between three gaseous signals for the 36 regulation of flooding survival and identifies novel regulatory targets for early stress 37 perception that could be pivotal for developing flood-tolerant crops. 38 39 42 cellular oxygen (O 2 ) deprivation (hypoxia) and survival strongly depends on molecular responses 43 that enhance hypoxia tolerance 2,3 . In submerged plant tissues the limited gas diffusion causes 44 passive ethylene accumulation. This rapid ethylene build-up can occur prior to the onset of 45 severe hypoxia, making it a timely and reliable signal for submergence 4,5 . In several plant 46 species, ethylene regulates adaptive responses to flooding involving morphological and 47anatomical modifications that prevent hypoxia 5 . Surprisingly, ethylene has so far not been 48 linked to metabolic responses that reduce hypoxia damage. In addition, how plants detect and 49 transduce early submergence signals to enhance survival remains elusive. 50 Here we show that plants can quickly detect submergence using passive ethylene accumulation 51 and integrate this signal to acclimate to subsequent hypoxia. This ethylene-mediated hypoxia 52 acclimation is dependent on enhanced ERFVII stability prior to hypoxia. We show that ethylene 53 limits ERFVII proteolysis under normoxic conditions by increasing the NO-scavenger 54 3 PHYTOGLOBIN1. Our results reveal a molecular mechanism that plants use to integrate early 55 stress signals to pre-adapt to forthcoming severe stress. 57 Results 58Early ethylene signalling enhances hypoxia acclimation 59 To unravel the spatial and temporal dynamics of ethylene signalling upon plant submergence, we 60 monitored the nuclear accumulation of ETHYLENE INSENSITIVE 3 (EIN3) 6-9 , an essential 61 transcription factor for mediating ethylene responses. We show, through an increase in EIN3- 62GFP fluorescence signal, that ethylene is rapidly perceived (within 1-2 h) in Arabidopsis 63 thaliana (hereafter Arabidopsis) root tips upon submergence (Supplementary Figure 1a-c). An 64 ethylene or submergence pre-treatment of only 4 hours was sufficient to increase root m...

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Section: Resultscontrasting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

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

Hartman

Liu

Veen

et al. 2019

Preprint

114

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“…These proteins (collectively the “MC‐ome”) represent diverse functions, many species specific, but a large number also conserved across flowering plants. Amongst these are three Met‐Cys initiating transcription‐associated protein types that have been shown to be bona fide substrates of the PCO branch of the PRT6 N‐degron pathway, the Group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factors (Gibbs et al ; Licausi et al ), the Polycomb Repressive Complex 2 component VERNALIZATION (VRN)2 (Gibbs et al ) and LITTLE ZIPPER 2 (ZPR2) transcription factor (Weits et al ). In all three cases it was shown physiologically that stability of the proteins is enhanced in hypoxia (reduced atmospheric oxygen) and genetically that this is mediated by the PRT6 N‐degron pathway.…”

Section: Protein Substrates Of the Plant N‐degron Pathwaysmentioning

confidence: 99%

“…In addition to the importance of correct responses to changes in external oxygen levels, a large body of work demonstrates that oxygen levels within plant tissues vary greatly that has regulatory consequences, for example in germ‐cell fate (Kelliher and Walbot ), suggesting that this may be an important determinant controlling metabolism and development. Recently a micro‐scale oxygen electrode was used to demonstrate that a steep oxygen gradient exists around the shoot apical meristem (SAM) of Arabidopsis and the distantly‐related asterid dicot Solanum lycopersicum , leading to very low meristem oxygen levels, that was not observed in the root meristem (Weits et al ). This was correlated with increased expression of core hypoxia genes within the SAM.…”

Section: Physiological Roles Of N‐degron Pathways In Plant Growth Andmentioning

confidence: 99%

The plant N‐degron pathways of ubiquitin‐mediated proteolysis

Holdsworth

Vicente

Sharma

et al. 2019

JIPB

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The amino-terminal residue of a protein (or amino-terminus of a peptide following protease cleavage) can be an important determinant of its stability, through the Ubiquitin Proteasome System associated N-degron pathways. Plants contain a unique combination of N-degron pathways (previously called the N-end rule pathways) E3 ligases, PROTEOLYSIS (PRT)6 and PRT1, recognizing non-overlapping sets of amino-terminal residues, and others remain to be identified. Although only very few substrates of PRT1 or PRT6 have been identified, substrates of the oxygen and nitric oxide sensing branch of the PRT6 N-degron pathway include key nuclear-located transcription factors (ETHYLENE RESPONSE FACTOR VIIs and LITTLE ZIPPER 2) and the histone-modifying Polycomb Repressive Complex 2 component VERNALIZATION 2. In response to reduced oxygen or nitric oxide levels (and other mechanisms that reduce pathway activity) these stabilized substrates regulate diverse aspects of growth and development, including response to flooding, salinity, vernalization (cold-induced flowering) and shoot apical meristem function. The N-degron pathways show great promise for use in the improvement of crop performance and for biotechnological applications. Upstream proteases, components of the different pathways and associated substrates still remain to be identified and characterized to fully appreciate how regulation of protein stability through the amino-terminal residue impacts plant biology.

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“…AtERF#111 is one of eight members of the subgroup X of the ERF/AP2 family (Nakano et al ., ). Recently, two other proteins with an N‐terminal MC motif, VERNALISATION2 (VRN2) (Gibbs et al ., ) and LITTLE ZIPPER 2 (ZPR2) (Weits et al ., ) were demonstrated to be oxygen‐sensitive targets of the Cys branch of the PRT6 N‐degron pathway, thereby linking oxygen availability to the epigenetic control of plant development and shoot meristem activity, respectively.…”

Section: Introductionmentioning

confidence: 99%

AtERF#111/ABR1 is a transcriptional activator involved in the wounding response

et al. 2019

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AtERF#111/ABR1 belongs to the group X of the ERF/AP2 transcription factor family (GXERFs) and is shoot specifically induced under submergence and hypoxia. It was described to be an ABA-response repressor, but our data reveal a completely different function. Surprisingly, AtERF#111 expression is strongly responsive to wounding stress. Expression profiling of ERF#111-overexpressing (OE) plants, which show morphological phenotypes like increased root hair length and number, strengthens the hypothesis of AtERF#111 being involved in the wounding response, thereby acting as a transcriptional activator of gene expression. Consistent with a potential function outside of oxygen signalling, we could not assign AtERF#111 as a target of the PRT6 N-degron pathway, even though it starts with a highly conserved N-terminal MetÀCys (MC) motif. However, the protein is unstable as it is degraded in an ubiquitin-dependent manner. Finally, direct target genes of AtERF#111 were identified by microarray analyses and subsequently confirmed by protoplast transactivation assays. The special roles of diverse members of the plant-specific GXERFs in coordinating stress signalling and wound repair mechanisms have been recently hypothesized, and our data suggest that AtERF#111 is indeed involved in these processes.For hypoxia treatments, 7-day-old seedlings grown on MS medium were used. 2 h after the onset of the photoperiod, open Petri dishes were placed into a desiccator for the indicated time periods

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An apical hypoxic niche sets the pace of shoot meristem activity

Cited by 175 publications

References 59 publications

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

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

The plant N‐degron pathways of ubiquitin‐mediated proteolysis

AtERF#111/ABR1 is a transcriptional activator involved in the wounding response

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