Diagnosis Of Plant Stress Caused By Dissolved Oxygen Concentration

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An insufficient supply of oxygen to the root has a negative effect in a number of metabolic processes, and its symptoms become visible, that is plants become wilted and defoliated (Morard and Silvestre, 1996), when they are irreversibly damaged (Klaring and Zude, 2009). Growth may be decreased and sometimes impaired under oxygen deficiency (Incrocci et al., 2000; Kogawara et al., 2006; Parelle et al., 2006; Taiz and Zeiger, 2002, p. 616; Wagner and Dreyer, 1997). Leaf growth is restricted (Incrocci et al., 2000; Pezeshki et al., 1996) and older leaves senesce prematurely because of reallocation of phloem mobile nutrients to younger leaves (Taiz and Zeiger, 2002, p. 618), hence, a reduction in plant leaf area. Root growth is limited (Mielke et al., 2003; Pezeshki et al., 1996; Smethurst et al., 2005) even more than shoot growth (Smethurst and Shabala, 2003), which increases the shoot/root ratio (Klaring and Zude, 2009). Therefore, it is very important to detect the stress caused by hypoxia in time to prevent further yield reductions or even plant death (Klaring and Zude, 2009). The effect of oxygen deficiency and subsequent recovery in plant tissues depends on the duration and severity of oxygen deprivation, tolerance of the species or cultivars to oxygen deficiency, age and developmental stage of the plant, type of tissue and light level and ambient temperature (Blokhina et al., 2003; Bragina et al., 2001; Fukao and Bailey-Serres, 2004; Klaring and Zude, 2009; Morard et al., 2000; Smethurst et al., 2005). Therefore, varied and sometimes contradictory plant responses have been recorded.

The most immediate effect of the decline of oxygen concentration in the root environment is that root aerobic respiration is seriously restricted (Islam and Macdonald, 2004; Taiz and Zeiger, 2002, p. 616). Pyruvate, the product of glycolysis, is then transformed to lactate, malic acid or mainly ethanol, which represent the main fermentation pathways in plants (Saenger, 2002; Sousa and Sodek, 2002). Fermentation involves a severe reduction of ATP synthesis that affects plant cell metabolism (Bertrand et al., 2003; Morard and Silvestre, 1996). It also leads to the accumulation of toxic compounds like ethanol or acetaldehyde (Klaring and Zude, 2009; Morard and Silvestre, 1996; Schmull and Thomas, 2004), but normally to levels that do not injure plant tissues (Lambers et al., 2008). Fermentation causes acidification of cytoplasm that decreases the activity of many enzymes, a possible cause of cell death (Vartapetian and Jackson, 1997). Despite its negative consequences, fermentation seems to ensure root survival under anaerobic conditions and it is very important for stress tolerance (Blokhina et al., 2003; Fukao and Bailey-Serres, 2004; Taiz and Zeiger, 2002, pp. 619620). The early induction of the ethanolic fermentation pathway and sugar utilization under hypoxia allows the maintenance of the energy status and, hence, improves anoxia tolerance (Blokhina et al., 2003). Acclimation to anaerobic conditions enhances the expression of genes that encode many of the anaerobic stress proteins, which are mainly related to enzymes of the glycolytic and fermentation pathways (Blokhina et al., 2003; Lambers et al., 2008; Taiz and Zeiger, 2002, p. 620). A high-activity fermentative enzyme alcohol dehydrogenase (ADH) has been measured in many plants, whether tolerant to hypoxia or not (Kogawara et al., 2006; Pezeshki et al., 1996; Weng and Chang, 2004), and it is considered an indicator of hypoxia in plants (Kogawara et al., 2006). The activity of enzyme sucrose synthase is also promoted under hypoxia with the aim of sustaining glycolytic flux (Klaring and Zude, 2009; Parelle et al., 2006). However, an inhibition of the sucrolytic, glycolytic and fermentative enzymes may occur under anoxia (Mustroph and Albrecht, 2003).

Fermentation accelerates the use of carbon reserves, so a prolonged period of oxygen deficiency may lead to the exhaustion of substrates (Bertrand et al., 2003). In order to protect root functions, plants tolerant to oxygen deficiency appear capable of sustaining photoassimilate transport to hypoxic roots (Kogawara et al., 2006). However, a reduction in distribution of photosynthates towards the roots has been reported in sensitive plants, which leads to an increased concentration of carbohydrates in the shoots (Islam and Macdonald, 2004; Kogawara et al., 2006) and may lead to feedback inhibition of photosynthesis (Smethurst et al., 2005). Once in the roots, photoassimilates may be partitioned among metabolic, structural and storage processes (Kogawara et al., 2006), the partitioning being metabolically available forms the most advisable to maintain a high energy status, as occurs in highly tolerant species (Kogawara et al., 2006). However, in sensitive species, root hypoxia might increase photoassimilate partitioning into the storage fraction and decrease partitioning to metabolic processes and structural components in roots (Kogawara et al., 2006).

As a result of the reduced root biomass (Smethurst et al., 2005) and the decrease of ATP in the roots due to the inhibition of aerobic respiration (Morard and Silvestre, 1996; Morard et al., 2004) and the lower import of photosynthates in the roots, the absorption of nutrients may decrease under oxygen deprivation (Smethurst et al., 2005; Taiz and Zeiger, 2002, p. 618; Vartapetian and Jackson, 1997). The depressive effects of oxygen deficiency on uptake have been classified by Morard and Silvestre (1996) in the following order: K > N > P > H2O > Mg-Ca. Potassium uptake is the most sensitive and even efflux has been observed soon after the exposition to oxygen deficiency (Morard et al., 2000). It has been attributed to depolarization of root cell membranes, a direct consequence of H+-ATPase inhibition (Mor-ard and Silvestre, 1996). In addition, a low concentration of oxygen in the root environment decreases the selectivity of K+/Na+ uptake in favour of Na+ and retards the transport of K+ to the shoots (Armstrong and Drew, 2002). Smethurst et al. (2005) observed nutrient deficiencies after 20 days of oxygen deficiency in Medicago sativa L. However, irreversible nutritional stress has not been detected in plants under these conditions (Morard and Silvestre, 1996).

Stomatal closure has been observed under root oxygen deficiency in many species (Bradford and Hsiao, 1982; Incrocci et al., 2000; Islam and Macdonald, 2004; Jackson and Hall, 1987; Kogawara et al., 2006; Mielke et al., 2003; Pezeshki et al., 1996; Schmull and Thomas, 2004; Weng and Chang, 2004; Yordanova and Popova, 2001; Yordanova et al., 2003) often associated with a high concentration of ABA in their tissues (Incrocci et al., 2000; Jackson and Hall, 1987; Sojka, 1992). This has been mostly attributed to the production of ABA by the older lower leaves that wilt and export their ABA to the younger leaves, where stomata close (Zhang and Zhang, 1994). In addition, roots may stimulate ABA production or reduce cytokinin synthesis (Morard and Silvestre, 1996) under oxygen deficiency. The decrease in stomatal conductance leads to a reduction of transpiration, water uptake and root hydraulic conductance (Islam and Macdonald, 2004; Jackson and Hall, 1987; Morard and Silvestre, 1996; Morard et al., 2000; Nicolas et al., 2005; Schmull and Thomas, 2004; Smethurst and Shabala, 2003; Vartapetian and Jackson, 1997; Weng and Chang, 2004; Yordanova and Popova, 2001; Yordanova et al., 2003; Yoshida et al., 1996). Unexpectedly, this has no negative consequence on leaf hydration since leaf water potential is unchanged (Bradford and Hsiao, 1982; Incrocci et al., 2000; Taiz and Zeiger, 2002, p. 618; Weng and Chang, 2004) or even increased (Jackson and Hall, 1987).

In addition to the effect of stomatal closure on transpiration, it also reduces CO2 intake and, thus, CO2 assimilation (Islam and Macdonald, 2004; Kogawara et al., 2006; Mielke et al., 2003; Mustroph and Albrecht, 2003; Pezeshki et al., 1996; Wagner and Dreyer, 1997). Nevertheless, some species tolerant to oxygen deficiency can sustain photosynthesis under root hypoxic conditions (Kogawara et al., 2006). In addition to stomatal closure, other non-stomatal factors may affect photosynthesis. For example, a reduction of RuBisCO content or activity (Panda et al., 2008; Yordanova and Popova, 2001; Yordanova et al., 2003) and a decrease in leaf chlorophyll content (Schlüter and Crawford, 2001; Smethurst and Shabala, 2003; Wagner and Dreyer, 1997; Yordanova and Popova, 2001) have been measured under oxygen deficiency. Also, changes in the profile of carotenoids may occur and, accordingly, Klaring and Zude (2009) suggested that the measurement of leaf diffuse reflectance in the carotenoids absorption bands (at 550 and 455 nm) may provide a sensitive tool of stress diagnosis under these conditions.

Photochemistry might also be affected by oxygen deprivation as a consequence of the lower CO2 assimilation rate (Mielke et al., 2003). Down-regulation of PSII has been measured by CF as an increase of non-photochemical quenching (Mielke et al., 2003; Schlüter and Crawford, 2001) usually coupled with a decrease in photochemical quenching (Schlüter and Crawford, 2001). In the long term, though, photochemistry may be affected by direct damage of components and membranes of the photosyn-thetic apparatus (Yordanova et al., 2003) or even by the nutrient deficiency caused by the impaired nutrient uptake (Smethurst et al., 2005). Then, the capacity for non-photochemical quenching may diminish, which leads to a permanent overexcitation of the thylakoids and enhanced danger of photo-inhibitory damage (Schlüter and Crawford, 2001). As a result, a decrease of Fv/Fm has been measured in some species under oxygen deficiency (Panda et al., 2008; Schlüter and Crawford, 2001; Smethurst and Shabala, 2003; Smethurst et al., 2005; Wagner and Dreyer, 1997). Fv/Fm and non-photochemical quenching have been considered as reliable indicators of tolerance to oxygen deficiency (Smethurst and Shabala, 2003; Smethurst et al., 2005).

In addition to the already explained consequences of oxygen deficiency, it also contributes to oxidative stress in plants. An in-depth review of oxidative stress in plants under oxygen deficiency has been made by Blokhina et al. (2003). Generation of ROS can take place in hypoxic tissues as a result of overreduction of redox chains under hypoxia and especially under reoxy-genation. Hence, anoxic stress is always accompanied to some extent by oxidative stress (Blokhina et al., 2003). Hydrogen peroxide accumulation under hypoxic conditions has been reported (Yordanova et al., 2003). In order to protect membranes integrity, the antioxidant system is stimulated by oxygen deficiency (Blokhina et al., 2003). For example, an increase in the activities of several antioxidant enzymes like CAT, APX or SOD (Biemelt et al., 1998; Yordanova et al., 2003) or a higher level of antioxidant compounds like ascorbate and glutathione (Biemelt et al., 1998) have been measured under oxygen deprivation.

After hypoxia and/or anoxia conditions, physiological functions can eventually be recovered (Morard and Silvestre, 1996; Panda et al., 2008; Schlüter and Crawford, 2001; Smethurst et al., 2005), although, sometimes, growth may remain reduced (Smethurst et al., 2005). This recovery may take different times depending on the duration of the stress or the tolerance of the species (Schlüter and Crawford, 2001) and might depend on the preservation of membrane integrity under anoxia (Blokhina et al., 2003). Under reoxygenation, plants suffer not only from weakening by anoxia stress but they also have to endure the formation of ROS (Schlüter and Crawford, 2001).

Plants may adapt to the lack of oxygen in the root environment by a mechanism called "nitrate respiration", where NO3~ is reduced in root cells to NO2~ by NR and acts as an alternative electron acceptor to O2 (Morard and Silvestre, 1996). This phenomenon has been observed in tomato when, after 12 hour of anoxia, nitrites were detected in the nutrient solution (Morard et al., 2000). An increase of NR activity has been also observed by Allegre et al. (2004) and Morard et al. (2004) under oxygen deficiency. Stoimenova et al. (2007) observed that mitochondria isolated from the roots of barley and rice seedlings were capable of oxidizing external nicotinamide adenine dinucleo-tide (NADH) and nicotinamide adenine dinucleotide phosphate (NADPH) anaerobically in the presence of nitrite. It has been suggested that nitrate reduction actually serves as an intermediate step of a respiratory pathway alternative to glycolytic fermentation: the haemoglobin (Hb)/nitric oxide (NO) cycle. In this cycle, NO produced from nitrate is oxidized back to nitrate in a reaction involving non-symbiotic Hb. The drop in ATP levels seems to stimulate the gene expression of Hb (Parelle et al., 2006), and enhance the activation of NR. The anaerobic ATP synthesis rate may be about 3-5% of the aerobic mitochondrial ATP synthesis rate (Stoimenova et al., 2007). For review see Igamberdiev and Hill (2004) and Igamberdiev et al. (2005).

To sum up, in order to carry out a reliable diagnosis of oxygen deficiency in plants, the following techniques can be used: measurements of biomass production and yield, shoot/root ratio, leaf area, root respiration, accumulation of ethanol and acetaldehyde, measurements of lipid peroxidation and ROS species, the amount of antioxidant compounds, photosynthetic activity, chlorophyll content, stomatal conductance, transpiration, water uptake, root hydraulic conductance, ABA accumulation, CF, content, type and partitioning of carbohydrates, leaf diffuse reflectance, nutrient uptake and measurements of the level, gene expression and/or activity of ADH, sucrose synthase, Hb, NR, RuBisCO or antioxidant enzymes.

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