Endogenous Hypoxia in Lateral Root Primordia Controls Root Architecture by Antagonizing Auxin Signaling in Arabidopsis

Shukla, Vinay; Lombardi, Lara; Iacopino, Sergio; Pěnčík, Aleš; Novák, Ondřej; Perata, Pierdomenico; Giuntoli, Beatrice; Licausi, Francesco

doi:10.1016/j.molp.2019.01.007

Cited by 107 publications

(111 citation statements)

References 78 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: 80%

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: 80%

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

Hartman

Liu

Veen

et al. 2019

Preprint

114

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“…NAC060, has been shown to be induced by the sugar-ABA signalling pathway. However, NAC060 availability in the nucleus hinders sugar-ABA signalling leading to seedlings' insensitivity to sugars 65 . A former study in rice showed that the link between low oxygen signals and the sugar-sensing cascade (via SnRK1) is important for regulation of sugar and energy production and therefore rice growth under flood conditions 66 .…”

Section: Regulated Transcription Factors Serve As Potential Targets Fmentioning

confidence: 99%

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Safavi-Rizi

Herde

Stöhr

2020

Sci Rep

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Due to climate change, economically important crop plants will encounter flooding periods causing hypoxic stress more frequently. this may lead to reduced yields and endanger food security. As roots are the first organ to be affected by hypoxia, the ability to sense and respond to hypoxic stress is crucial. At the molecular level, therefore, fine-tuning the regulation of gene expression in the root is essential for hypoxia tolerance. Using an RnA-Seq approach, we investigated transcriptome modulation in tomato roots of the cultivar 'Moneymaker', in response to short-(6 h) and long-term (48 h) hypoxia. Hypoxia duration appeared to have a significant impact on gene expression such that the roots of five weeks old tomato plants showed a distinct time-dependent transcriptome response. We observed expression changes in 267 and 1421 genes under short-and long-term hypoxia, respectively. Among these, 243 genes experienced changed expression at both time points. We identified tomato genes with a potential role in aerenchyma formation which facilitates oxygen transport and may act as an escape mechanism enabling hypoxia tolerance. Moreover, we identified differentially regulated genes related to carbon and amino acid metabolism and redox homeostasis. Of particular interest were the differentially regulated transcription factors, which act as master regulators of downstream target genes involved in responses to short and/or long-term hypoxia. Our data suggest a temporal metabolic and anatomic adjustment to hypoxia in tomato root which requires further investigation. We propose that the regulated genes identified in this study are good candidates for further studies regarding hypoxia tolerance in tomato or other crops.

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“…There is therefore a link between osmotic and oxidative stress, root formation and the activity of this group of genes. It has recently been shown that hypoxic niches are generated during the formation of lateral roots in Arabidopsis, which leads to the induction of ERF-VII genes, which in turn modulate the auxin response in the developing tissue (Shukla et al 2019). Moreover, this hypoxic environment has also been detected in the shoot apical meristem, where oxygen acts as a diffusible signal that controls development (Weits et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Expression of a Rap2.12 like-1 ERF gene during adventitious rooting of chestnut and oak microshoots

Valladares¹,

Varas²,

Vielba

et al. 2020

Israel J. Plant Sci.

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Adventitious rooting of cuttings is a complex developmental process in forest species, with several exogenous and endogenous factors influencing the outcome of the process. In this study we applied an in vitro working system, comprising two lines of microshoots with the same genotype but at a different ontogenetic stages, in two different tree species (chestnut and oak). We analyzed the expression of a gene encoding an AP2/ERF transcription factor from group VII in the initial hours of the adventitious rooting induction, both in rooting competent and incompetent microshoots. The analysis revealed that expression of this gene is related to wounding, ontogenetic stage and auxin in a complex and species-specific manner. Putative induction of the gene by auxin was also analyzed in the presence of naphthyl-phthalamic acid (NPA), an auxin transport inhibitor. In situ expression analysis in chestnut relates the gene activity to cambial divisions and root primordia in rooting competent microshoots, as well as in the root apex. The putative role of the gene during adventitious roots formation is discussed.

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Endogenous Hypoxia in Lateral Root Primordia Controls Root Architecture by Antagonizing Auxin Signaling in Arabidopsis

Cited by 107 publications

References 78 publications

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

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

RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root

Expression of a Rap2.12 like-1 ERF gene during adventitious rooting of chestnut and oak microshoots

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