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      Ethylene Differentially Modulates Hypoxia Responses and Tolerance across Solanum Species

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          Abstract

          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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          Most cited references42

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          Prioritizing climate change adaptation needs for food security in 2030.

          Investments aimed at improving agricultural adaptation to climate change inevitably favor some crops and regions over others. An analysis of climate risks for crops in 12 food-insecure regions was conducted to identify adaptation priorities, based on statistical crop models and climate projections for 2030 from 20 general circulation models. Results indicate South Asia and Southern Africa as two regions that, without sufficient adaptation measures, will likely suffer negative impacts on several crops that are important to large food-insecure human populations. We also find that uncertainties vary widely by crop, and therefore priorities will depend on the risk attitudes of investment institutions.
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            The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water.

            Living organisms must acquire new biological functions to adapt to changing and hostile environments. Deepwater rice has evolved and adapted to flooding by acquiring the ability to significantly elongate its internodes, which have hollow structures and function as snorkels to allow gas exchange with the atmosphere, and thus prevent drowning. Many physiological studies have shown that the phytohormones ethylene, gibberellin and abscisic acid are involved in this response, but the gene(s) responsible for this trait has not been identified. Here we show the molecular mechanism of deepwater response through the identification of the genes SNORKEL1 and SNORKEL2, which trigger deepwater response by encoding ethylene response factors involved in ethylene signalling. Under deepwater conditions, ethylene accumulates in the plant and induces expression of these two genes. The products of SNORKEL1 and SNORKEL2 then trigger remarkable internode elongation via gibberellin. We also demonstrate that the introduction of three quantitative trait loci from deepwater rice into non-deepwater rice enabled the latter to become deepwater rice. This discovery will contribute to rice breeding in lowland areas that are frequently flooded during the rainy season.
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              Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization.

              The majority of eukaryotic organisms rely on molecular oxygen for respiratory energy production. When the supply of oxygen is compromised, a variety of acclimation responses are activated to reduce the detrimental effects of energy depletion. Various oxygen-sensing mechanisms have been described that are thought to trigger these responses, but they each seem to be kingdom specific and no sensing mechanism has been identified in plants until now. Here we show that one branch of the ubiquitin-dependent N-end rule pathway for protein degradation, which is active in both mammals and plants, functions as an oxygen-sensing mechanism in Arabidopsis thaliana. We identified a conserved amino-terminal amino acid sequence of the ethylene response factor (ERF)-transcription factor RAP2.12 to be dedicated to an oxygen-dependent sequence of post-translational modifications, which ultimately lead to degradation of RAP2.12 under aerobic conditions. When the oxygen concentration is low-as during flooding-RAP2.12 is released from the plasma membrane and accumulates in the nucleus to activate gene expression for hypoxia acclimation. Our discovery of an oxygen-sensing mechanism opens up new possibilities for improving flooding tolerance in crops. © 2011 Macmillan Publishers Limited. All rights reserved
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                Author and article information

                Journal
                Plants (Basel)
                Plants (Basel)
                plants
                Plants
                MDPI
                2223-7747
                13 August 2020
                August 2020
                : 9
                : 8
                : 1022
                Affiliations
                Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands; n.s.vandongen@ 123456students.uu.nl (N.v.D.); d.m.h.j.renneberg@ 123456uu.nl (D.M.H.J.R.); R.A.M.Welschen@ 123456uu.nl (R.A.M.W.-E.); johanna.kociemba@ 123456crick.ac.uk (J.K.)
                Author notes
                Author information
                https://orcid.org/0000-0002-6709-6436
                https://orcid.org/0000-0003-0313-8972
                Article
                plants-09-01022
                10.3390/plants9081022
                7465973
                32823611
                42bcd127-2078-48c6-8177-a276677c6207
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 24 July 2020
                : 10 August 2020
                Categories
                Article

                ethylene,flooding,hypoxia,phytoglobin,vii ethylene response factor,prt6 n-degron pathway of proteolysis,solanum tuberosum,solanum lycopersicum,solanum dulcamara

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