Chapter 4 Low Oxygen Signaling and Tolerance in Plants

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Abstract

Plants often experience low-oxygen conditions, not only as an environmental stress condition but also as part of their normal developmental process. Oxygen deficiency signaling in the plant cell has been shown to involve reactive oxygen and nitrogen species, hormones, and calcium as secondary messengers, similarly to the low-oxygen signaling observed in other eukaryotic systems. However, in plants, evidences suggesting the existence on an oxygen sensor are scant. To date, research efforts have been aimed at understanding the strategies used by plants to low oxygen. Anatomical modifications, which encompass leaf elongation, adventitious rooting production and aerenchyma formation, can help the plants to avoid the stress consequent to low oxygen availability. On the other hand, metabolic adaptations enable the plant tissue to survive while experiencing oxygen deficiency, mainly coupling structural maintenance with energy saving. Application of the knowledge already available to crops may provide solutions for both agricultural and industrial processes involving low-oxygen conditions.

Section snippets

Introduction: Plant Cells Dealing with Low Oxygen

The Earth is the only planet in the solar system with an oxygen rich atmosphere. Evolving biological organisms have developed mechanisms that link efficient energy production with oxygen availability. This has made life on earth strictly dependent on oxygen not only for energy production but also for a number of different biochemical reactions. However, oxygen limitations are a normal part of the developmental process, especially in multicellular organisms which, as a consequence, have

Oxygen Sensing in Eukaryots

To achieve rapid and highly tuneable responses, oxygen signaling should rely on one or more sensors capable of immediately perceiving when oxygen concentrations fall below a critical level and should be able to trigger different responses depending on the organ, tissue or cell type. A number of direct and indirect sensors probably represent the best solution to cope with a dynamic stress situation, such as a slow shift from hypoxia to complete anoxia through increasingly harsh hypoxic

Oxygen Sensors in Plants

It is still unknown how plants do sense oxygen. Different hypotheses have been provided, involving direct oxygen binding or metabolism. However, while some of them have been excluded from the plethora of candidates for the oxygen sensing, others still need to be characterized. Indirect sensing, via signal compound(s) accumulated during oxygen shortage, is also likely to contribute to trigger or modulate the hypoxic response in the plant cell.

Gibbs and Greenway (2003) raised the question whether

Low-Oxygen Signal Transduction in Plants

The search for signaling components in low-oxygen plant responses has been carried out mostly using genetic approaches; although some reverse genetic approaches have provided encouraging results. Provided the relatively vast amount of data on the hypoxic response at the transcriptional level, the easiest starting points with respect to the search for signal transducer have been the functional analysis of induced proteins known to be involved in signaling in other conditions, or sharing homology

Low-Oxygen Related Stresses: Energy Deficits and Consequences

The main cellular stress caused by low oxygen availability consists in a reduced respiration and, therefore, lower energy production, resulting in slower metabolic processes. Recently, studies in pea and Arabidopsis roots suggested that plant cell adjust respiration to oxygen availability to prevent, or at least postpone, anoxia (Zabalza et al., 2009). When respiratory activity is reduced or blocked, energy production is limited to the glycolytic process. To avoid slowing in the glycolytic

Metabolic Adaptation to Energy Crisis

When plants, or some of their organs, cannot avoid hypoxic conditions, they try to metabolically adapt to cope with the stress.

As mentioned previously, energy production under anaerobic conditions mainly depends on the glycolytic pathway, which, in turn, requires the regeneration of NAD+. As respiration is reduced, pyruvate is rapidly accumulated in concentrations similar to the Km of pyruvate decarboxylase (PDC), whose affinity for the substrate is usually lower than that of pyruvate

Dealing with Oxygen Shortages: Avoidance Strategies

To avoid the energy crisis caused by oxygen deprivation, plants developed a number of constitutive or inducible tolerance strategies depending on their growing environment. Plant species that experience periodic and long-lasting flooding (e.g., Rumex palustris and Ranunculus sceleratus) and species able to germinate in flooded soils (e.g., O. sativa and Potagemoton pectinaus) have indeed evolved a number of strategies that enable photosynthetic tissues to reach the surface of the water and

Functional Maintenance of the Cell and Energy Saving

Cell survival under oxygen deprivation relies on the ability to maintain a minimal functionality that minimizes energy costs and sustains membrane integrity and cellular compartmentation. To cope with the energy crisis, ATP-expensive processes such as protein synthesis are strongly reduced, while the limited amount of ATP produced is used to counteract the detrimental cytosolic acidification by fuelling the H+ transport to the vacuole. Presence of anaerobic proteins preceding an anoxic stress

Conclusions

Oxygen sensing and signal transduction in plants is undoubtedly much less explored when compared to other eukaryotes. However, advances in analysis techniques together with the increasing interest in applications of low-oxygen treatments in crop science and technology have recently contributed considerably to a better understanding of the molecular mechanisms underlying plant adaptation to anaerobiosis. Exponential increase in genome sequences for crop plants is also extremely beneficial,

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