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      Low Oxygen Response Mechanisms in Green Organisms

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          Abstract

          Low oxygen stress often occurs during the life of green organisms, mostly due to the environmental conditions affecting oxygen availability. Both plants and algae respond to low oxygen by resetting their metabolism. The shift from mitochondrial respiration to fermentation is the hallmark of anaerobic metabolism in most organisms. This involves a modified carbohydrate metabolism coupled with glycolysis and fermentation. For a coordinated response to low oxygen, plants exploit various molecular mechanisms to sense when oxygen is either absent or in limited amounts. In Arabidopsis thaliana, a direct oxygen sensing system has recently been discovered, where a conserved N-terminal motif on some ethylene responsive factors (ERFs), targets the fate of the protein under normoxia/hypoxia. In Oryza sativa, this same group of ERFs drives physiological and anatomical modifications that vary in relation to the genotype studied. The microalga Chlamydomonas reinhardtii responses to low oxygen seem to have evolved independently of higher plants, posing questions on how the fermentative metabolism is modulated. In this review, we summarize the most recent findings related to these topics, highlighting promising developments for the future.

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          Most cited references184

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          Genome-wide analysis of the ERF gene family in Arabidopsis and rice.

          Genes in the ERF family encode transcriptional regulators with a variety of functions involved in the developmental and physiological processes in plants. In this study, a comprehensive computational analysis identified 122 and 139 ERF family genes in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa L. subsp. japonica), respectively. A complete overview of this gene family in Arabidopsis is presented, including the gene structures, phylogeny, chromosome locations, and conserved motifs. In addition, a comparative analysis between these genes in Arabidopsis and rice was performed. As a result of these analyses, the ERF families in Arabidopsis and rice were divided into 12 and 15 groups, respectively, and several of these groups were further divided into subgroups. Based on the observation that 11 of these groups were present in both Arabidopsis and rice, it was concluded that the major functional diversification within the ERF family predated the monocot/dicot divergence. In contrast, some groups/subgroups are species specific. We discuss the relationship between the structure and function of the ERF family proteins based on these results and published information. It was further concluded that the expansion of the ERF family in plants might have been due to chromosomal/segmental duplication and tandem duplication, as well as more ancient transposition and homing. These results will be useful for future functional analyses of the ERF family genes.
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            Flooding stress: acclimations and genetic diversity.

            Flooding is an environmental stress for many natural and man-made ecosystems worldwide. Genetic diversity in the plant response to flooding includes alterations in architecture, metabolism, and elongation growth associated with a low O(2) escape strategy and an antithetical quiescence scheme that allows endurance of prolonged submergence. Flooding is frequently accompanied with a reduction of cellular O(2) content that is particularly severe when photosynthesis is limited or absent. This necessitates the production of ATP and regeneration of NAD(+) through anaerobic respiration. The examination of gene regulation and function in model systems provides insight into low-O(2)-sensing mechanisms and metabolic adjustments associated with controlled use of carbohydrate and ATP. At the developmental level, plants can escape the low-O(2) stress caused by flooding through multifaceted alterations in cellular and organ structure that promote access to and diffusion of O(2). These processes are driven by phytohormones, including ethylene, gibberellin, and abscisic acid. This exploration of natural variation in strategies that improve O(2) and carbohydrate status during flooding provides valuable resources for the improvement of crop endurance of an environmental adversity that is enhanced by global warming.
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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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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                Molecular Diversity Preservation International (MDPI)
                1422-0067
                March 2013
                27 February 2013
                : 14
                : 3
                : 4734-4761
                Affiliations
                [1 ]PlantLab, Institute of Life Sciences, Scuola Superiore Sant’Anna, Via Mariscoglio 34, Pisa 56124, Italy; E-Mails: v.banti@ 123456sssup.it (V.B.); b.giuntoli@ 123456sssup.it (B.G.); s.gonzali@ 123456sssup.it (S.G.); g.novi@ 123456sssup.it (G.N.); e.paparelli@ 123456sssup.it (E.P.); s.parlanti@ 123456sssup.it (S.P.); c.pucciariello@ 123456sssup.it (C.P.); a.santaniello@ 123456sssup.it (A.S.)
                [2 ]Institute of Agricultural Biology and Biotechnology, National Research Council, Via Moruzzi 1, Pisa 56100, Italy; E-Mail: loreti@ 123456ibba.cnr.it
                [3 ]Institute of Plant Biochemistry and Biotechnology, University of Münster, Schlossplatz 8, Münster 48143, Germany; E-Mail: magneschi@ 123456uni-muenster.de
                Author notes
                [* ]Author to whom correspondence should be addressed; E-Mail: pierdomenico.perata@ 123456sssup.it ; Tel.: +39-050-221-1585.
                Article
                ijms-14-04734
                10.3390/ijms14034734
                3634410
                23446868
                ebd97bc7-8012-441a-843b-c87224ca991c
                © 2013 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 license ( http://creativecommons.org/licenses/by/3.0/).

                History
                : 29 January 2013
                : 20 February 2013
                : 21 February 2013
                Categories
                Review

                Molecular biology
                anoxia,arabidopsis thaliana,chlamydomonas reinhardtii,hypoxia,low oxygen,n-end rule,oryza sativa

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