Regulation of the molecular response to oxygen ... - Wiley Online Library

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Minireview Regulation of the molecular response to oxygen limitations in plants Author for correspondence: Francesco Licausi Tel: +31 331 5678353 Email: [email protected]

Francesco Licausi Max Planck Institute of Molecular Plant Physiology, Energy Metabolism Research Group, Am Mu¨hlenberg 1, D–14476, Potsdam-Golm, Germany

Received: 31 August 2010 Accepted: 17 October 2010

Summary New Phytologist (2011) 190: 550–555 doi: 10.1111/j.1469-8137.2010.03562.x

Key words: anoxia, ethylene, ethylene responsive factor (ERF), hypoxia, oxygen, reactive nitrogen species (RNS), reactive oxygen species (ROS).

The oxygen availability to plant tissues can vary strongly in time and space. To endure short- or long-term oxygen deprivation, plants evolved a series of metabolic and morphological adaptations that have been extensively studied. However, our knowledge of the molecular regulation of these processes is not as well understood. In this review, the recent findings on the molecular effectors that regulate the response of higher plants to oxygen deficiency are discussed. Although no direct oxygen sensor has been discovered in plants so far, mechanisms that perceive low-oxygen derived signals have been reported, involving different sets of transcription factors (TFs). The ERF (Ethylene Responsive Factor) family especially appears to play a crucial role in the determination of survival to reduced oxygen availability in Arabidopsis and rice. This class of TFs displays a broad range of targets, being involved in both the metabolic reprogramming and the morphological adaptations exploited by plants when subjected to low-oxygen conditions.

Low oxygen condition in plants Plants, like any other aerobic organisms, require molecular oxygen as electron acceptor for respiratory energy metabolism. However, because of a reduced availability of oxygen from the environment during flooding or water-logging, and because of the diffusion resistance of plant tissues for oxygen growing under normal aerobic conditions, plant cells have to cope with highly variable and often limiting oxygen concentrations (Licausi & Perata, 2009). Reduced oxygen availability to cells can either be described as hypoxia or as anoxia. The term anoxia is used for a situation in which no oxygen is available for the cell at all. De facto, this restrains the respiratory energy production and ATP is mainly produced by glycolysis. By contrast, hypoxia describes a partial reduction of the oxygen availability. Under these conditions, cells are still able to produce ATP

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via oxidative phosphorylation, but the rate of oxygen consumption is reduced and cells optimize energy usage by reorganizing metabolic fluxes (Rocha et al., 2010). As a result of efficient metabolic adaptations to hypoxia, moderate changes in the plant internal oxygen concentration do not necessarily reflect severe stress but are suggested to play a role in the regulation of growth and development (Mustroph et al., 2009).

Adaptive responses to oxygen deprivation Prolonged energy shortage in the cells would ultimately compromise survival of the plant. To avoid this, plants have developed various morphological strategies to improve oxygen supply to hypoxic tissues, as well as metabolic adaptations to save energy and thus oxygen (Bailey-Serres & Voesenek, 2008).

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New Phytologist Formation of air-filled porous tissue called aerenchyma to facilitate gas exchange (Armstrong & Drew, 2002), production of adventitious roots in nonsubmerged areas of the stem (Vidoz et al., 2010) and rapid elongation to escape the water level (Nagai et al., 2010) are the most important morphological adaptations exploited by plants growing under oxygen limitation (Licausi & Perata, 2009). Plant hormones, and especially ethylene, play a pivotal role in the regulation of these modifications. Ethylene production is stimulated by hypoxia in Arabidopsis seedlings and accumulates within tissues during flooding because of the reduced diffusion rates of gases into the surrounding water (Hinz et al., 2010; Peng et al., 2010). Ethylene induces programmed cell death to generate aerenchyma (Drew et al., 2003) and elicits the formation of adventitious roots via positive-feedback on auxins (Vidoz et al., 2010). Ethylene also stimulates cell expansion and promotes the degradation of abscisic acid which ultimately leads to the stimulation of cell division by gibberellins (GAs) (BaileySerres & Voesenek, 2008). The best-investigated metabolic response to hypoxia is the induction of fermentation, and further metabolic adaptations include the inhibition of storage metabolism and a shift to energy efficient pathways, for example to those that consume pyrophosphate (PPi) rather than ATP (Huang et al., 2008).

Low-oxygen perception and signaling The tight control of biochemical, physiological and morphological adaptation to low oxygen suggests that a finely-tuned oxygen sensing and signaling pathway must exist in plants. However, unlike for animals, fungi and prokaryotes (Semenza, 2004; Hughes & Espenshade, 2008; Unden et al., 2010), the mechanism by which oxygen levels are perceived in plants remains unknown. It is debated whether plants can sense oxygen concentrations directly or rather respond to variations in the concentration of metabolic parameters that directly or indirectly depend on the oxygen availability such as energy charge, pH and reactive oxygen or nitrogen species (ROS and RNS, respectively) (Licausi & Perata, 2009). A partial overlap between the molecular response to energy depletion and to hypoxia was observed in Arabidopsis thaliana by Baena-Gonza´lez et al. (2007). This subset of genes appeared to be regulated by the protein kinases AKIN10 and AKIN11, plant homologues of the yeast sucrose nonfermenting related kinases (SnRKs) known as metabolic sensors for glucose or the ATP : AMP ratio and involved in adjusting the energy homeostasis (Baena-Gonza´lez et al., 2007). Experiments with rice revealed more kinases to be involved in hypoxic signaling: OsCIPK15, a calcineurin Blike (CBL)-interacting protein kinase, activates another kinase, SnRK1A that, in turn, induces a MYB-type transcription factor (TF), MYBS1 (Lee et al., 2009). MYBS1 is


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responsible for the upregulation of an a-amylase (Ramy3D) that catalyses the hydrolysis of starch during hypoxia (Lee et al., 2009). In addition, CIPK15 was shown to be required for the upregulation of both the alcohol dehydrogenase genes (OsADH1 and OsADH2) during hypoxia in rice (Lee et al., 2009). The contribution of ROS to low oxygen signaling is suggested by the observation that the production of hydrogen peroxide (H2O2) and lipid peroxidation increase upon hypoxia in several plant species (Blokhina & Fagerstedt, 2010). In Arabidopsis, the anaerobic production of H2O2 by means of a NADPH oxidase is required for the induction of the ADH gene (Baxter-Burrell et al., 2002). Indeed, two NADPH oxidases (RBOHD and RBOHF) are induced by hypoxia in Arabidopsis (van Dongen et al., 2009). The reversible activation of a calcium dependent NADPH oxidase is mediated by a RHO-like small G protein of plants (Rop protein) and was shown to be necessary for tolerance to oxygen deprivation in Arabidopsis seedlings (BaxterBurrell et al., 2002). Not only ROS peak upon hypoxia, nitric oxide (NO) production also increases when the oxygen availability goes down as a result of increased nitrite reduction to NO, either by the enzyme nitrate reductase or as a result of the usage of nitrite as alternative final electron acceptor in the mitochondrial electron transport chain (Igamberdiev & Hill, 2009). However, the latter pathway only occurs under strict anoxic conditions.

The molecular response to low oxygen in plants Several genome-wide analyses contributed to generate a detailed overview of the various molecular responses ranging from the role of TFs (Licausi et al., 2010b), to profiling of gene expression (Lasanthi-Kudahettige et al., 2007; van Dongen et al., 2009) and translation (Branco-Price et al., 2008) that take place under oxygen depletion in plants. The number and type of genes induced or repressed under low oxygen conditions seems to depend on the extent of the oxygen depletion (van Dongen et al., 2009). Transcriptomewide analyses of Arabidopsis and rice seedlings under anoxic conditions showed the induction of transcripts to be related to ROS detoxification, and protein- or membrane-stabilization such as ascorbate peroxidase (APX) and heat shock proteins (HSPs) (Loreti et al., 2005; Lasanthi-Kudahettige et al., 2007; Branco-Price et al., 2008; Narsai et al., 2009; Jung et al., 2010). In Arabidopsis, these genes are not induced when a slight amount of oxygen is still present (Licausi et al., 2010b). By contrast, another group of c. 50 genes is induced when the oxygen concentration decreased only partly. Within this core set of hypoxia-induced genes, several encode fermentation enzymes, or proteins involved in the scavenging of toxic byproducts of fermentation (van Dongen et al., 2009). However, almost 70% of the core-

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responsive genes code for proteins for which no function has been determined yet. Time-resolved analyses of the hypoxic response in Arabidopsis roots showed a rapid response within 30 min of a small number of genes, mostly encoding for proteins with undetermined function (van Dongen et al., 2009). However, after 48 h of hypoxia most of these induced mRNA returned to normoxic levels (van Dongen et al., 2009), suggesting that the plant tissues either reached a new homeostatic condition or attenuated specific short-term hypoxic responses. As the mRNAs of anaerobic core-responsive genes were found to be associated with polysomes under anoxia in Arabidopsis seedlings, it is assumed that they are actively translated (Branco-Price et al., 2008). Indeed, proteome analyses of soybean root tissues treated with waterlogging confirmed an increase in fermentative and glycolytic enzymes, but highlighted a discrepancy between the abundance of transcript and protein that belong to other functional categories (Komatsu et al., 2009). It is likely that ribosomes bind to specific transcripts to be prepared for rapid translation upon reoxygenation. Alternatively, it is possible that some specific proteins are constantly degraded under normoxic conditions but stabilized during hypoxic conditions. Selective induction of protein synthesis upon hypoxia or reoxygenation likely represents a crucial point in the adaptation of cells to oxygen deficiency. A rapid relocation of the ATP-binding protein DEAD box protein eIF4A-III, a core component of the exon junction complex (ECJ) in the nucleolus and splicing speckles, was observed in Arabidopsis and tobacco cells after 1 h hypoxia (Koroleva et al., 2009). The ECJ is involved in the translation enhancement of spliced mRNA under stress conditions (Ma et al., 2008). It has been speculated that upon energy shortage most of the eIF4A-III molecules would not be bound by ATP thus assuming a favorable conformation to assemble on mRNA substrates (Koroleva et al., 2009).

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Cell-specific responses to oxygen deprivation at the translational level were recently investigated in Arabidopsis seedlings by Mustroph et al. (2009) using an epitope-tagged ribosomal protein expressed under the control of tissuespecific promoters. This study confirmed the core set of genes that is ubiquitously upregulated under hypoxia, and revealed cell- and organ-specific responses involved in specialized processes. Interestingly, hypoxia-responsive mRNAs were already highly abundant under normoxic conditions in phloem cells, confirming the physiological hypoxic condition of the vascular tissue (van Dongen et al., 2003). Conversely, heat shock proteins (HSP) and ROS-related transcripts were not elevated in the phloem, supporting the hypothesis that the induction of these genes involves a specific response to absolute anoxia.

Regulators of the molecular response to hypoxia in plants The regulation of the molecular response to low oxygen involves various TFs. Over 180 TF genes were found to be up regulated or downregulated in Arabidopsis roots under hypoxic conditions most of which belonged to ERF (Ethylene Response Factor), bHLH, MYB, bZIP and Zinc Finger families. However, HSF and ZAT TFs seem to constitute a specific response to anoxia (Licausi et al., 2010b). Comparison of TF activity between different plant species revealed several homologous TF genes being induced by low oxygen conditions such as members of the ERFs family, the Lateral Organ Boundary Domain proteins (LBDs) and trihelix proteins (Licausi & Perata, 2009). The best characterized regulators of plant adaptive responses to flooding-induced anaerobiosis are members of the ERF subfamily VII (Nakano et al., 2006). Despite their acronym, not all of these genes respond to ethylene and now the name is used to describe proteins that contain at least one copy of the family-specific DNA binding domain. One flooding-

(b) Fig. 1 Sequence comparisons of Arabidopsis and rice Ethylene Responsive Factor (ERF) transcription factors (TFs) belonging to group VII. (a) Comparison of the amino acid sequence of the conserved N-terminal motif in ERF-VII proteins of Arabidopsis thaliana (Col-0) and rice (Oryza sativa japonica and indica varieties). The ERF TFs that affect flooding tolerance in rice are highlighted in bold. Shaded boxes represent different levels of conservation among the ERF VII proteins in Arabidopsis (black, 100%; dark tint, 80%; light tint, 60%). (b) Phylogenetic tree illustrating the relation of group VII ERFs in Arabidopsis and rice.



New Phytologist tolerance inducing ERF TF is SUB1A, which occurs specifically in indica varieties of rice (Xu et al., 2006). SUB1A directly or indirectly activates Slender-rice 1 (SLR1) and SLR1-like 1 (SLRL1) which in turn repress the GAenhanced elongation of internodes in submerged rice plants. This energy-saving strategy allows the plant to avoid unnecessary use of energy and saves nutrient resources for the post-submergence phase (Fukao & Bailey-Serres, 2008). The alternative strategy adopted by deep-water rice varieties specifically improves tolerance to submergence periods of some weeks to several months. It relies on fast elongation of the internodes to stretch out the leaves above the water surface. This response was shown to be coordinated by the ERF TFs Snorkel1 (SK1) and Snorkel2 (SK2) (Hattori et al., 2009). Both these genes act downstream of the ethylene signaling cascade and are direct targets of the TF Ethylene-Insensitive-3 (EIN-3) (Hattori et al., 2009). It is suggested that the molecular mechanisms by which SK1 and SK2 regulate internode elongation may act via increasing the sensitivity of the tissues to endogenous GA or via changing the concentration of active gibberellins (Nagai et al., 2010). Interestingly, all the ERFs that are involved in the flooding tolerance (SK1, SK2, SUB1A and SUB1C) distinguish themselves from the other members of the ERFVII group by variation in the highly conserved N-terminal motif (MCGGAI ⁄ L; Fig. 1), suggesting a specific function of this domain in the protein family. However, the exact role of this motif remains to be investigated. In Arabidopsis, homologues of SUB1A and SK1 and SK2 are also involved in the tolerance response to anoxia and hypoxia. Among the five Arabidopsis members of the ERFVII group, the transcript level of HRE1 and HRE2 strongly increases during oxygen depletion (Licausi et al., 2010a). However, this induction is regulated via different mechanisms: for HRE1 increased transcriptional activity appeared to be responsible, whereas mRNA stabilization of constitutively expressed HRE2 resulted in increased transcript levels of this gene (Licausi et al., 2010a). Overexpression of HRE1 increased and accelerated the induction of anaerobic genes including HRE2 under hypoxia, but had almost no effect on the expression of the same genes under normoxic conditions (Licausi et al., 2010a). Transgenic Arabidopsis seedlings overexpressing either HRE1 or HRE2 showed increased tolerance to anoxia (Fig. 2). Double hre1hre2 knock-out mutants but not single hre1 or hre2 mutants showed a decrease in the expression of several hypoxia-genes after 2 h when compared with the wild-type. This indicates that these two genes are redundant for maintaining the expression of the whole set of anaerobic genes under prolonged oxygen limitation (Fig. 3). Whereas expression of the Hypoxia Responsive ERF (HRE) TFs is not affected by ethylene, other members of the same subfamily, RAP2.2 and RAP2.3 are induced by ethylene. Ethylene seems also to be required to trigger the induction of


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Fig. 2 Effect of knocking-out or overexpressing Hypoxia Responsive ERF (HRE) transcription factors (TFs) on Arabidopsis thaliana seedling growth during normoxia (Control; a, c) or after 8 h or 10 h of anoxia followed by a 2-wk recovery period (Anoxia; b, d, respectively). The double knockout hre1 hre2 is unable to survive the anoxic treatment anymore, whereas constitutive overexpression of either HRE1 or HRE2 increased seedling survival significantly. Adapted from Licausi et al. (2010a).

Fig. 3 General model of the low oxygen signal transduction in plants. Oxygen deficiency is perceived via either ethylene or reactive oxygen species (ROS) : reactive nitrogen species (RNS) signals or via yet unknown sensor mechanism and this leads to the induction of Ethylene Responsive Factor (ERF), Lateral Organ Boundary Domain (LBD), trihelix, Heat Shock Factors (HSF) and Zinc finger of Arabidopsis thaliana (ZAT) transcription factors. Hypoxia- and ethylene-induced ERFs cooperate with unknown TFs to trigger and maintain the induction of genes encoding enzymes involved in anaerobic metabolism. Hypoxia-induced ethylene accumulation regulates growth and elongation either in positive or negative manner depending on a tolerance specific genetic asset of ERF factors available in the plant genome. Under anoxic conditions, a specific subset of TFs induces genes involved in the amelioration of oxidative stress.

ADH under hypoxic conditions in Arabidopsis (Peng et al., 2001). Over-expression of RAP2.2 enhances the expression of a subset of hypoxic genes in leaf tissues under hypoxia and improves the tolerance to oxygen limitations in Arabidopsis grown on nutrient medium (Hinz et al., 2010). Interestingly, the ERF-VII TFs contain a potential recognition site


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for the ATCTA DNA motif that is over-represented in the promoter regions of most of the hypoxia-responsive genes (Licausi et al., 2010b). A transactivation assay showed that this motif is indeed involved in the regulation of transcription, as HRE1 was able to activate transcription through interaction with the ADH and Hb1 promoters, both containing the ACTCA elements (Licausi et al., 2010b). Although transactivation assays revealed evidence for the regulatory role of ERF TF in hypoxic Arabidopsis, overexpression of any of the Arabidopsis ERF-VII genes did not change the expression of anaerobic core-genes under normoxia. Therefore, it is likely that the simultaneous action of a subset of TFs is required to induce high expression of hypoxia-induced genes. Apart from the ERF-VII group, some other TFs have also been reported to play a role in the hypoxic response. The Arabidopsis MYB2-protein was the first TF to be suggested to be linked to the regulation of anaerobic genes by activating the ADH promoter via binding to the GT-motif (Hoeren et al., 1998). However, myb2 knock-out mutants did not show differences in the expression of anaerobic genes compared with wild type (Licausi et al., 2010a). Possibly, redundancy with other MYB TFs can explain this neutral phenotype. Other TFs reported to play a role in the response to low oxygen in Arabidopsis are the NAC protein, ANAC102, which activates a seed-specific subset of genes during germination under oxygen limitations (Bond et al., 2009), and VIN3 (Vernalization-Independent 3), which mediates chromatin rearrangements required for plant survival. However,VIN3 does not affect expression of the hypoxic core-response genes (Christianson et al., 2009). Members of the DOF, bZIP and Zinc Finger families represent possible regulators, as they are able to bind elements in the promoter regions of ADH or Hb1 (Licausi et al., 2010b). Not only TFs are important to regulate molecular responses to low oxygen. Trans-acting small RNAs, such as the small interfering RNAs (siRNAs) and microRNAs (miRNAs) have been shown to play an important role in the post-transcriptional regulation of gene expression. Genome-wide analyses led to the identification 34 siRNAs and 25 miRNAs that are differentially regulated upon anoxia (Moldovan et al., 2009, 2010). However, detailed time-resolved analyses showed that most of the anoxic responsive miRNAs are not upregulated under moderate oxygen depletion (Licausi et al., 2010b). Moreover, large discrepancies became evident between the expression of miRNA precursor genes and the abundance of their final product, suggesting the existence of a post-transcriptional mechanism (Licausi et al., 2010b). Unfortunately, the target mRNA of the miRNAs that were shown to respond to hypoxia are not yet known and those that are predicted by in silico tools do not show significant differences in transcript abundance (Licausi et al., 2010b). Possibly these


miRNAs act at the translational level blocking ribosome progression along the messenger, but further research is required to learn more about the role of miRNAs in the regulation of the molecular responses to low oxygen.

Conclusions and future perspectives The recent discoveries of various signaling components of the low-oxygen sensing pathway allow the drafting of an overview of several factors involved in the regulation of the molecular response to oxygen deprivation in plants (Fig. 3). The oxygen signaling mechanism is able to distinguish between a partial reduction in the oxygen availability and the absolute absence of oxygen. Specific subsets of TFs are activated either directly (via ethylene or ROS and RNS) or indirectly (probably via a sensor for molecular oxygen),. The synergic interaction of various combinations of TF then positively or negatively regulates the expression of a core set of low-oxygen genes that renders metabolic and morphological adaptations to the oxygen deficiency (Fig. 3). In summary, during the last 5 yr, our knowledge of the oxygen sensing and signaling cascades has greatly improved. However, the revelation of the molecular sensor that perceives actual changes in the oxygen concentration within plant tissues remains a quest for the future. The analysis of interaction partners and upstream regulators of the proteins recently identified as hypoxic effectors in rice and Arabidopsis constitute a promising means to ultimately achieve this goal.

Acknowledgements I am very grateful to Joost T. van Dongen and Pierdomenico Perata for their support and advice in writing this manuscript. I apologize to colleagues whose work could not be included because of limited space.

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