Chapter Five - New Insights into the Metabolic and Molecular Mechanism of Plant Response to Anaerobiosis

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Abstract

Under anaerobic conditions, plants apply a wide spectrum of precise adaptive strategies responding to several critical challenges. The ability of efficiently sensing the oxygen presence demonstrates the existence of both direct and indirect ways of perception. The subsequent coordinate metabolic reassessment is currently under study. The complex molecular response implicates not only transcriptional and translational regulation of specific genes but also posttranscriptional and posttranslational regulatory mechanisms, each and all integrating the metabolic settings. Furthermore, the accumulation of typical metabolites during low oxygen stress condition is a key factor that suggests some critical topics in the regulation of metabolic pathways. Here, we summarize the main routes for adaptive behavior during oxygen depletion, from oxygen availability perception to recently discovered molecular mechanisms and metabolic adaptations.

Introduction

The Geologic Calendar is a scale in which the age of the Earth is assumed to be as long as 1 year. While Homo sapiens appears on the Earth in the last 4 min of this year, land plants cover the entire last month. This point of view may suggest the extent to which plants demonstrate an ability to recognize and face the wide variety of environmental conditions, even stressful and drastic, bypassing their main limit—being sessile—and colonizing the planet. Plant distinctive feature refers not only to the unavoidable necessity to face conditions without escape but also to the spread and unpredictability of seed dispersion, insomuch as second-generation plants can grow in environmental conditions that are completely different from those of their parent plants.

Both of these challenges led to the evolvement of a wide spectrum of adaptive strategies, insofar as a single plant may produce changes in metabolism in order to face an environmental state or a transient condition, inducing different metabolic responses depending on the degree of the stress conditions and involving the whole plant in a coordinated response. In particular, soil flooding—and thus anaerobiosis—is a stress condition that requires quick and precise sensing, well-coordinated signaling and an integrative response in order to bypass the stress without irreversibly impairing cell metabolism.

In responding to oxygen depletion at the molecular level, a main role has been observed for both transcriptional and translational regulations of specific genes, such as the hypoxia-related transcription factors (TFs)—in particular the family VII of the ERF (ethylene response factor) and heat shock transcription factors (HSFs), involved in oxygen sensing and stress response triggering (Licausi and Perata, 2009, Licausi et al., 2011, Pucciariello et al., 2012).

Furthermore, recent studies have highlighted the even higher complexity of this molecular response; posttranscriptional and posttranslational regulations also participate in the network of regulatory mechanisms (Mazzucotelli et al., 2008), integrating the modulation of metabolic settings. The metabolic and physiological reassessment induced by the lack of oxygen also depends on indirect sensing mechanisms involving different changes in cytosolic parameters and hormonal balances (Bailey-Serres et al., 2012). From a metabolic point of view, production of lactate and ethanol has been studied since 1974 when Davies and colleagues suggested the mechanisms regulating lactic and ethanolic fermentation.

More recently, studies of the accumulation of specific amino acids were found to belong to the adaptive response of the plant to the lack of oxygen. In particular, alanine and γ-aminobutyric acid (GABA) have been found to be the most biosynthesized amino acids during hypoxic conditions, with a role in maintaining the osmotic potential and in limiting the cytosolic acidification (Miyashita and Good, 2008). Succinate also accumulates, suggesting the last step of the noncircular TCA cycle active during oxygen depletion (Sweetlove et al., 2010), while the observed production of γ-hydroxybutyrate (GHB) during stress has been explained with the conversion of succinic semialdehyde derived from GABA-T by means of a specific reductase enzyme (Breitkreuz et al., 2003, Deleu et al., 2013, Renault et al., 2012).

Furthermore, metabolic adaptations also involve a mitochondrial role for nitrite, where it acts as an alternative electron acceptor in the electron transport chain, producing nitric oxide (Stoimenova et al., 2007) and contributing to the maintenance of mitochondrial activity and ATP synthesis during anoxic conditions (Igamberdiev et al., 2005, Stoimenova et al., 2007). Thus, plant strategies for adaptation to low oxygen conditions are defined by a complex coordination of molecular, metabolic, and physiological redefinitions, which allow the survival of plants even under strict low oxygen conditions.

Section snippets

Roots

Roots are very sophisticated organs; they ceaselessly maintain a highly complex interdependent relationship with biotic and abiotic components of soil. While root apparatus is strongly influenced by the environment, it also strongly influences the surrounding soil by means of exudates, water and oxygen uptake, and metabolic activities (Hinsinger et al., 2009). Furthermore, also among those processes operating inside roots, there is an interdependence that involves soil condition, soil condition

Molecular Mechanisms in Anaerobic Response

During hypoxic and anoxic stress, plant adaptive strategies have been divided into two broad groups: low oxygen quiescence syndrome (LOQS) and low oxygen escape syndrome (LOES) (Colmer and Voesenek, 2009). However, some responses have been shown to be conserved in all flooding-adapted plants, independently from the strategy. Since oxygen availability becomes low during submergence, plants following the LOQS strategy reduce or repress stem elongation and keep metabolic pathways in a quiescent

Metabolic Adaptations

Anoxic stress induces rapid and severe metabolic and molecular adaptations in order to confront the fall in ATP production, due to the lack of oxygen as the final acceptor of electrons in oxidative phosphorylation, the fall in cytosolic pH, and the imbalance in osmotic potential. There is evidence about changes in enzyme composition in the cytosol and in mitochondria (Couee et al., 1992, Igamberdiev and Hill, 2009, Igamberdiev et al., 2004, Miyashita and Good, 2008), mainly related to the

Concluding Remarks

Recent advances in plant strategies to survive anaerobic conditions gain knowledge about specific plant adaptive responses, increasing the understandig of how sensing, signaling, and thus response can quickly and successfully coordinate. The integrate regulation of molecular, metabolic, and physiological responses allows the plant survival even under strict low oxygen conditions.

Observation and deep analysis have highlighted different levels of the survival strategy, such as transcriptional and

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