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

Hartman, Sjon; Liu, Zeguang; Veen, Hans van; Vicente, Jorge; Reinen, Emilie; Martopawiro, Shanice; Zhang, Hongtao; Dongen, Nienke van; Bosman, F.; Bassel, George W.; Visser, Eric J. W.; Bailey‐Serres, Julia; Theodoulou, F. L.; Hebelstrup, Kim H.; Gibbs, Daniel J.; Holdsworth, Michael J.; Sasidharan, Rashmi; Voesenek, Laurentius A. C. J.

doi:10.1038/s41467-019-12045-4

Cited by 235 publications

(220 citation statements)

References 44 publications

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“…Ethylene production during B. cinerea infection (Chaqu e et al, 2002) could have two consequences. On the one hand, it may contribute to induce the expression of ERF-VII at the transcriptional level (Hinz et al, 2010;Hartman et al, 2019), and on the other, it could enhance ERF-VII stability before hypoxia by increasing expression of the NO-scavenger PGB1 (Hartman et al, 2019). We observed production of ETH in the plants infected with B. cinerea (Fig.…”

Section: Researchmentioning

confidence: 73%

Botrytis cinerea induces local hypoxia in Arabidopsis leaves

et al. 2020

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Low oxygen availability often is associated with soil waterlogging or submergence, but may occur also as hypoxic niches in otherwise aerobic tissues. Experimental evidence assigns a role in Botrytis cinerea resistance to a group of oxygen-unstable Ethylene Response Factors (ERF-VII). Given that infection by B. cinerea often occurs in aerobic organs such as leaves, where ERF-VII stability should be compromised, we explored the possibility of local leaf hypoxia at the site of infection.We analyzed the expression of hypoxia-responsive genes in infected leaves. Confocal microscopy was utilized to verify the localization of the ERF-VII protein RAP2.12. Oxygen concentration was measured to evaluate the availability of oxygen (O 2 ).We discovered that infection by B. cinerea induces increased respiration, leading to a drastic drop in the O 2 concentration in an otherwise fully aerobic leaf. The establishment of a local hypoxic area results in stabilization and nuclear relocalization of RAP2.12. The possible roles of defence elicitors, ABA and ethylene were evaluated.Local hypoxia at the site of B. cinerea infection allows the stabilization of ERF-VII proteins. Hypoxia at the site of pathogen infection generates a nearly O 2 -free environment that may affect the stability of other N-degron-regulated proteins as well as the metabolism of elicitors.

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Section: Researchmentioning

confidence: 73%

Botrytis cinerea induces local hypoxia in Arabidopsis leaves

et al. 2020

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“…In addition, passive ethylene entrapment acts as a rapid signal for submergence, and regulates many flood adaptive responses that include morphological and anatomical modifications to prevent hypoxia [8]. Ethylene also mediates metabolic hypoxia acclimation in the wetland species Rumex palustris and the model species Arabidopsis (Arabidopsis thaliana) [9][10][11]. In Arabidopsis, ethylene-mediated hypoxia tolerance is conserved in root and shoot meristems and is associated with enhanced expression of a conserved set of hypoxia-responsive genes when O 2 levels decline [10,12].…”

Section: Introductionmentioning

confidence: 99%

“…Ethylene also mediates metabolic hypoxia acclimation in the wetland species Rumex palustris and the model species Arabidopsis (Arabidopsis thaliana) [9][10][11]. In Arabidopsis, ethylene-mediated hypoxia tolerance is conserved in root and shoot meristems and is associated with enhanced expression of a conserved set of hypoxia-responsive genes when O 2 levels decline [10,12]. These hypoxia adaptive genes are predominantly controlled by the group VII Ethylene Response Factor (ERFVII) transcription factors RELATED TO APETALA2.2 (RAP2.2), RAP2.12 and RAP2.3 [13,14].…”

Section: Introductionmentioning

confidence: 99%

“…When the cellular levels of either O 2 or NO decline, ERFVII proteolysis is restricted and these proteins stabilize, ultimately activating target hypoxia adaptive gene expression [24][25][26]. Ethylene can already stabilize ERFVIIs prior to hypoxia through active NO reduction, by enhancing levels of the NO-scavenging protein PHYTOGLOBIN1 (PGB1) [10]. In addition, ethylene can promote ERFVII production through transcriptional activation.…”

Section: Introductionmentioning

confidence: 99%

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Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

Hartman

Dongen

Renneberg

et al. 2020

Plants

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The increasing occurrence of floods hinders agricultural crop production and threatens global food security. The majority of vegetable crops are highly sensitive to flooding and it is unclear how these plants use flooding signals to acclimate to impending oxygen deprivation (hypoxia). Previous research has shown that the early flooding signal ethylene augments hypoxia responses and improves survival in Arabidopsis. To unravel how cultivated and wild Solanum species integrate ethylene signaling to control subsequent hypoxia acclimation, we studied the transcript levels of a selection of marker genes, whose upregulation is indicative of ethylene-mediated hypoxia acclimation in Arabidopsis. Our results suggest that ethylene-mediated hypoxia acclimation is conserved in both shoots and roots of the wild Solanum species bittersweet (Solanum dulcamara) and a waterlogging-tolerant potato (Solanum tuberosum) cultivar. However, ethylene did not enhance the transcriptional hypoxia response in roots of a waterlogging-sensitive potato cultivar, suggesting that waterlogging tolerance in potato could depend on ethylene-controlled hypoxia responses in the roots. Finally, we show that ethylene rarely enhances hypoxia-adaptive genes and does not improve hypoxia survival in tomato (Solanum lycopersicum). We conclude that analyzing genes indicative of ethylene-mediated hypoxia acclimation is a promising approach to identifying key signaling cascades that confer flooding tolerance in crops.

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“…Recent studies have demonstrated that when submergence is established, gas diffusion of ethylene is restricted, and it is trapped in the plant, triggering its signaling pathway at early submergence. When submergence is prolonged, ethylene synthesis is reduced due to hypoxia; group VII ethylene response factor (ERFVII) activity is activated by hypoxia signaling [30][31][32]. In our previous reports, we demonstrated that the NADPH oxidase RbohD plays a major role in the early stages of hypoxic stress responses.…”

Section: Discussionmentioning

confidence: 99%

NADPH Oxidase RbohD and Ethylene Signaling are Involved in Modulating Seedling Growth and Survival Under Submergence Stress

Hong

Wang

Yang

2020

Plants

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In higher plants under low oxygen or hypoxic conditions, the phytohormone ethylene and hydrogen peroxide (H2O2) are involved in complex regulatory mechanisms in hypoxia signaling pathways. The respiratory burst oxidase homolog D (RbohD), an NADPH oxidase, is involved in the primary stages of hypoxia signaling, modulating the expression of downstream hypoxia-inducible genes under hypoxic stress. In this study, our data revealed that under normoxic conditions, seed germination was delayed in the rbohD/ein2-5 double mutant, whereas postgermination stage root growth was promoted. Under submergence, the rbohD/ein2-5 double mutant line had an inhibited root growth phenotype. Furthermore, chlorophyll content and leaf survival were reduced in the rbohD/ein2-5 double mutant compared with wild-type plants under submerged conditions. In quantitative RT-PCR analysis, the induction of Ethylene-responsive factor 73/hypoxia responsive 1 (AtERF73/HRE1) and alcohol dehydrogenase 1 (AtADH1) transcripts was lower in the rbohD/ein2-5 double mutant during hypoxic stress than in wild-type plants and in rbohD and ein2-5 mutant lines. Taken together, our results indicate that an interplay of ethylene and RbohD is involved in regulating seed germination and post-germination stages under normoxic conditions. Moreover, ethylene and RbohD are involved in modulating seedling root growth, leaf chlorophyll content, and hypoxia-inducible gene expression under hypoxic conditions.

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

Cited by 235 publications

References 44 publications

Botrytis cinerea induces local hypoxia in Arabidopsis leaves

Botrytis cinerea induces local hypoxia in Arabidopsis leaves

Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

NADPH Oxidase RbohD and Ethylene Signaling are Involved in Modulating Seedling Growth and Survival Under Submergence Stress

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