AOBPreview originally published online on April 27, 2006
Annals of Botany 2006 98(1):9-32; doi:10.1093/aob/mcl076
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
INVITED REVIEW |
Conditions Leading to High CO2 (>5 kPa) in Waterlogged–Flooded Soils and Possible Effects on Root Growth and Metabolism
1 School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley 6009, WA, Australia and 2 Biological Sciences, University of Hull, Kingston upon Hull HU6 7RX, UK
* For correspondence. E-mail hank{at}cyllene.uwa.edu.au
Received: 27 September 2005 Returned for revision: 9 December 2005 Accepted: 9 February 2006 Published electronically: 27 April 2006
 |
ABSTRACT |
|---|
TOP
ABSTRACT
INTRODUCTION• Aims Soil waterlogging impedes gas exchange with the atmosphere, resulting in low PO2 and often high PCO2. Conditions conducive to development of high PCO2 (5–70 kPa) during soil waterlogging and flooding are discussed. The scant information on responses of roots to high PCO2 in terms of growth and metabolism is reviewed.
• Scope PCO2 at 15–70 kPa has been reported for flooded paddy-field soils; however, even 15 kPa PCO2 may not always be reached, e.g. when soil pH is above 7. Increases of PCO2 in soils following waterlogging will develop much more slowly than decreases in PO2; in soil from rice paddies in pots without plants, maxima in PCO2 were reached after 2–3 weeks. There are no reliable data on PCO2 in roots when in waterlogged or flooded soils. In rhizomes and internodes, PCO2 sometimes reached 10 kPa, inferring even higher partial pressures in the roots, as a CO2 diffusion gradient will exist from the roots to the rhizomes and shoots. Preliminary modelling predicts that when PCO2 is higher in a soil than in roots, PCO2 in the roots would remain well below the PCO2 in the soil, particularly when there is ventilation via a well-developed gas-space continuum from the roots to the atmosphere. The few available results on the effects of PCO2 at > 5 kPa on growth have nearly all involved sudden increases to 10–100 kPa PCO2; consequently, the results cannot be extrapolated with certainty to the much more gradual increases of PCO2 in waterlogged soils. Nevertheless, rice in an anaerobic nutrient solution was tolerant to 50 kPa CO2 being suddenly imposed. By contrast, PCO2 at 25 kPa retarded germination of some maize genotypes by 50 %. With regard to metabolism, assuming that the usual pH of the cytoplasm of 7·5 was maintained, every increase of 10 kPa CO2 would result in an increase of 75–90 mM HCO3– in the cytoplasm. pH maintenance would depend on the biochemical and biophysical pH stats (i.e. regulatory systems). Furthermore, there are indications that metabolism is adversely affected when HCO3– in the cytoplasm rises above 50 mM, or even lower; succinic dehydrogenase and cytochrome oxidase are inhibited by HCO3– as low as 10 mM. Such effects could be mitigated by a decrease in the set point for the pH of the cytoplasm, thus lowering levels of HCO3– at the prevailing PCO2 in the roots.
• Conclusions Measurements are needed on PCO2 in a range of soil types and in roots of diverse species, during waterlogging and flooding. Species well adapted to high PCO2 in the root zone, such as rice and other wetland plants, thrive even when PCO2 is well over 10 kPa; mechanisms of adaptation, or acclimatization, by these species need exploration.
Key words: Acid load, aerenchyma, bicarbonate, carbon dioxide, cytochrome c, O2 deficiency, pH regulation, metabolism, respiration, waterlogging, wetland plants
‘What is known about this?’ said the King.
‘Very little’ said Alice.
‘That is very important’ said the King.
(paraphrased from Alice's Adventures in Wonderland by Lewis Carroll)
|
INTRODUCTION |
|---|
Owing to the 104 times slower gas diffusion in water than in air, waterlogged soils are usually anoxic and by inference the slow gas diffusion will lead to accumulation of large amounts of dissolved inorganic carbon (Fig. 1; Armstrong, 1979
; Jackson and Drew, 1984). Consequently, many waterlogged soils are likely to increase in PCO2 to maxima between 10 and 40 kPa (equilibrium pressure; see Appendix 1 for abbreviations and definitions of terms used within the text) and sometimes higher, but these maxima would be reached much slower than the concurrent decrease in PO2 of the soil, owing to the combination of a 
34-fold higher solubility of CO2 than of O2 in aqueous media (Armstrong, 1979) and the conversion of a substantial proportion of CO2 to HCO3–, which will be particularly prominent at higher soil pH (Fig. 2). Hence, the present theme is clearly relevant to long-term flooding in marshes and wetlands, as well as in rice paddies; nevertheless, substantial PCO2 may also be reached in some types of soil during transient waterlogging lasting longer than several days.
|
|
In waterlogged soils, the cortical gas-space continuum in plants provides the principal pathway for O2 flow from the air to the roots, while in many cases zones receiving sufficient O2 for oxidative phosphorylation are adjacent to anoxic zones (Jackson and Armstrong, 1999
; Gibbs and Greenway, 2003). O2 movement and anaerobic metabolism have been reviewed elsewhere (for aeration: Jackson and Armstrong, 1999; Armstrong and Drew, 2002; Colmer and Greenway, 2005; for anaerobic metabolism: Armstrong and Drew, 2002; Gibbs and Greenway, 2003; Greenway and Gibbs, 2003; Jackson and Ricard, 2003). The present review evaluates the occurrence of high CO2 in waterlogged soils and the consequences for growth and metabolism of roots in such soils; as well as possible acclimatizions and adaptations to PCO2 in the range of 5–50 kPa, which have been measured in several flooded soils (Boru et al., 2003; IRRI, 2005). Surprisingly, plant responses to high PCO2 in waterlogged-flooded soils have hardly been studied. As a gross observation, wetland plants clearly thrive during flooding. For example, paddy rice in a field at IRRI (Philippines), with water depths maintained between 50 and 100 mm above the soil surface until 7 d before maturity, yielded up to 9·3 t ha–1 (Ying et al., 1998); this soil had a pH of 6·6 and 1·4 % organic matter and, as will be described shortly, would presumably have been at high PCO2, at least when rice was in its tillering stage.
A preliminary model, presented in this review, predicts that, even at 40 kPa CO2 in the soil, PCO2 in the roots would not often rise above 13–26 kPa. Nevertheless, even in plant organs surrounded by air some tissues may reach high PCO2 owing to restricted ventilation, as found in the xylem of stems of several tree species. Maximum values are particularly relevant to our theme, as these indicate what PCO2 the cells surrounding the xylem have to tolerate. These maximum values for CO2 in the xylem depend on the species; the range for maxima in different species was found to be 4–26 kPa CO2 (McGuire and Teskey, 2004). High PCO2 can also occur in some seed pods; in chickpea, CO2 during part of the day was zero, but 7–11 kPa CO2 was reached during the night (Ma et al., 2001). These data indicate that some germinating seeds might be tolerant to high PCO2 during flooding, because they require tolerance to high PCO2 during their formation.
Mechanisms by which wetland plants acclimatize to high PCO2 in the root zone have not been elucidated, and it is not clear to what extent there are adverse effects on non-wetland plants. Nevertheless, we can speculate on the consequences of the acid load exerted by high PCO2. Taking for the quasi steady state an example of a moderate PCO2 of 10 kPa, either HCO3– in the cytoplasm would be 75–90 mM (Table 1b), running the risk of adverse effects on metabolism, or the cytoplasm would have to be below the usual value of pH 7·5 (Table 1b). By analogy, a new set point for pH of the cytoplasm (pHcyt) has been suggested for energy-deficient cells (Felle, 1996, 2005; Greenway and Gibbs, 2003). Under anoxia, pHcyt usually decreases to between 6·9 and 7·1, even in anoxia-tolerant tissues (Greenway and Gibbs, 2003); the known exception is Potamogeton pectinatus in which pHcyt only decreased to 7·3 upon imposition of anoxia (Summers et al., 2000). So, in most species, the HCO3– concentrations in the cytoplasm, at a given PCO2, should be 2·5–4 times less for anoxic than for aerobic cells. In wetland species, with root systems containing large volumes of aerenchyma, the vast majority of cells would be expected to receive adequate O2 for oxidative phosphorylation (Armstrong and Drew, 2002; Colmer and Greenway, 2005), so whether these cells would also have a lower set point for pHcyt than when the roots are in an aerobic soil/medium is an intriguing question.
|
The scarce information on the effects of PCO2 higher than 5 kPa on metabolism is also reviewed here. Substantial information is available on exposure of fruits to high PCO2, but the relevance of these data to our theme is tenuous as these responses are confounded by effects of the climacteric.
We conclude that studies on growth and metabolism of roots at high PCO2 are required for wetland and non-wetland species, both for tissues with sufficient O2 for oxidative phosphorylation and for anoxic tissues.
|
PCO2 IN WATERLOGGED SOILS |
|---|
Few PCO2 values have been measured in waterlogged field soils. In one study, PCO2 increased from 1 to 30–35 kPa after 2 weeks of flooding (Boru et al., 2003
; crop was soybean, pH of soil, temperature and water depth above the soil were not reported). Changes in PCO2 of soils in pots have been evaluated, with the most comprehensive data set for 31 paddy-field soils without plants (IRRI, 2005; republished data obtained by Ponnamperuma in the 1960s). As expected, rises in PCO2 were rather gradual, while PCO2 declined again after 2–4 weeks of flooding (Fig. 3). This study indicated some trends for different groups of soil (table with Fig. 3). Peaks in PCO2 remained lower when soil pH started on the alkaline side, with maxima between 8–22 kPa in the alkaline soils and 15–40 kPa in mildly acidic soils (group 1 vs. group 2 in table with Fig. 3). There are also indications that during the first weeks of flooding, PCO2 may reach as high as 55 kPa in some soils that had an initial pH of between 4·6 and 5·5 and 70 kPa in some soils with a high percentage of organic matter (groups 3 and 4, respectively, in table with Fig. 3). PCO2, in all the types of soils, declined after prolonged flooding, although some soils still contained 24–36 kPa after 16 weeks of flooding (table with Fig. 3). There are also some experimental data from pots with plants. In an experiment with rice, trends in PCO2 upon flooding were similar to those shown in Fig. 3 (Cho and Ponnamperuma, 1971). Furthermore, the importance of soil pH was demonstrated: liming a sandy loam increased the original pH of 4·8 to 6·2; the average PCO2 over 2–4 weeks of flooding was 40 kPa for the limed soil and 60 kPa for the unlimed soil (Cho and Ponnamperuma, 1971; average of the soils at 20 and 30 °C). The data of Cho and Ponnamperuma (1971) were obtained by titrations using methyl orange as an indicator, and so more direct measurements of PCO2 are required. In an experiment with wheat, the PCO2 in soil following waterlogging to the soil surface rose over 6 d from 2 to 10 kPa; after another 4 d it had risen to 14 kPa – temperature was 14 °C, organic matter was 3·3 % and initial pH was 6·3 (Trought and Drew, 1980a; PCO2 measurement using a sample of soil solution and measuring the equilibrium CO2 in the gas head-space by gas chromatography). Rises in PCO2 after the start of waterlogging were much more gradual than the decreases in PO2; PO2 commonly decreases from 21 to 0 kPa within 1–1·5 d after the start of waterlogging (Trought and Drew, 1980a). A fast decline in soil PO2 after the onset of waterlogging is consistent with calculations showing that sealing the surface would deplete the O2 present in a (previously) well-aerated soil within 2 d (Payne and Gregory, 1988).
|
The increase in PCO2 in waterlogged soils (as shown for flooded soils in Fig. 3) would be associated with CO2 evolution during catabolism by micro-organisms, mediated by organic electron acceptors, as in alcoholic fermentation (Kirk, 2004
). Additional CO2 evolution would be derived from conversion of end products of anaerobic catabolism to CO2, mediated by inorganic electron acceptors, sequentially NO3–, Mn(III/IV) and then, as a principal acceptor, Fe(III) (Kirk, 2004). Usually, the CO2 production by the soil slows with time of flooding, and CO2 production is outstripped by factors decreasing PCO2, as shown after 2–4 weeks of flooding in Fig. 3.
One cause of CO2 removal would be loss to the atmosphere. The soil depth from which CO2 production is lost to the atmosphere would be greater the lower the CO2 production by the soil and the higher the PCO2 in the soil (Fig. 4). The percentage production lost from the soil profile can be derived by dividing the depths shown in Fig. 4 by the depth of the soil profile producing CO2. Taking a soil depth of 200 mm, as in rice paddies, then at 40 kPa in the soil the losses would be 12·5 and 6·5 % for CO2 production rates of 15 and 52 x 10–12 mol cm–3 s–1, respectively; at 10 kPa these losses would be only 6·2 and 3·5 %, respectively. Removals would be lessened for flooded soils. For example, CO2 removals would be reduced by at least half in rice paddies, with say 100 mm stagnant water on the soil surface. Reductions would be larger the higher the rate of CO2 production by the soil and at 10 vs. 40 kPa CO2 in the soil (Fig. 4). As an example, for a PCO2 in the soil of 10 kPa, and a production rate of 52 x 10–12 mol cm–3 s–1, losses from a 200-mm soil layer would become trivial, i.e. 0·5 % of the rate of production. These estimates are based on a Dsoil = 0·2D0, Dsoil is the effective CO2 diffusion coefficient in the soil and D0 is the CO2 diffusion coefficient in solution. Given that the thickness of the soil layer from which the CO2 is lost to the atmosphere varies with the square root of Dsoil, losses from a soil with a Dsoil of 0·33, a usual figure for a rice paddy, would be 1·3 times greater than given above.
|
In addition to atmospheric losses, other important factors causing CO2 in the soil to decline would be precipitation of inorganic carbon as complexes of Fe (Kirk, 2004
) and, in soils acidic at the start of flooding, increases in soil pH. The pH of the solution of rice paddy soils after 2 weeks of flooding usually ranges between 6·5 and 7·0, although there were cases reported when pH remained as low as 5·0 or as high as 8·0 (Ponnamperuma, 1984), so that CO2/HCO3– ratios would have been 25 and 0·02, respectively. Soils that are acidic at the start of waterlogging are likely to develop high PCO2 upon waterlogging faster than more alkaline soils (table with Fig. 3). In a survey of soils from paddy fields in Asia, the mean soil pH was 
5·5 in five of 11 countries (De Datta, 1981). Soils with a pH 5·5 or lower, including acid sulfate soils which occur in the deltas of south-east Asia (De Datta, 1981), would be particularly prone to develop high PCO2, particularly as some acid soils still had a pH of between 4·5 and 6·2 at 2 weeks after the start of flooding (Ponnamperuma, 1984). Furthermore, as discussed further below, CO2 exposure of rice roots growing in acidic soils would be increased due to biogeochemical reactions following radial loss of O2 from the roots to the soil, resulting in a lower pH in the rhizosphere and hence higher CO2 concentrations relative to the bulk soil. Thus, inorganic carbon accumulation as a result of flooding would intensify any acid load imposed by the acidity of these soils.
The time sequences for changes in PCO2 in the rice paddy soils shown in Fig. 3 can be compared with the known CO2 production rates in 16 anaerobic rice soils in a laboratory experiment at 30 °C (Yao et al., 1999). We deduce that the lowest CO2 production rates over the first 14 d of waterlogging would be 1·6 µmol g–1 d. wt soil d–1 and these rates would result in an increase in PCO2 of 4·0 kPa d–1, with about double that value for the mean production rate of the 16 soils (for procedures see Appendix 3b). By comparison, the observed increases were, on average, 1·6 kPa d–1 for the four rice paddy soils studied by Ponnamperuma (1984) with a range of 0·7–2·5 kPa (Fig. 3). This discrepancy may to some extent be due to the assumption of a soil porosity of 50 % (in Appendix 3b), while some paddy soils had total porosities of 61–62 % (Painuli et al., 1988) and heavy textured soils may change into a gel-like structure upon puddling and then increase in total porosity (Greenland, 1981); values of 60–70 % are typical for these soils (G. J. D. Kirk, pers. comm.). A total porosity of 70 rather than 50 % would reduce the assessed increase in PCO2 of 4·0 kPa d–1 to 2·9 kPa d–1. The remaining substantial discrepancy between the data on CO2 production and the observed increases in PCO2 of soils can be resolved only in comprehensive experiments designed to assess CO2 production rates, pH changes during waterlogging, total porosity of the particular soils, as well as monitoring any losses of CO2 from the soil.
The key data on soil PCO2 of Ponnamperuma (Fig. 3 and its table) were only for fallow soils, so it is crucial to obtain data for soils in the field carrying stands of rice. Roots would make a substantial contribution to the changes with time in PCO2 of the soil, in the early phase after the start of flooding CO2 production may contribute to the rate of rise in dissolved inorganic carbon in soils. Of equal importance, in the quasi steady state, the gas-space continua in the plants might vent, to the atmosphere, considerable amounts of CO2 that enter from the soil, in addition to the CO2 produced by the root's catabolism. Some indication for the importance of this venting can be gained from data on CH4 emissions: in a field ‘covered with rice’, cutting the rice stems below the water surface showed that up to 94 % of the methane emissions from the soil–root system was via the gas-space continua from roots to shoots (Holzapfel-Pschorn et al., 1986). In this quasi steady state, soil PCO2 will be determined by both the CO2 production by the soil and ventilation via the root system. That ventilation via plants depends on the density of roots of the stand was indicated by the very similar CH4 emission rates between soil with paddy rice and bare soil during the first 7 weeks after transplanting, when there would not yet be a dense stand (Holzapfel-Pschorn et al., 1986). Even when the bulk soil has reached a PCO2 of 40 kPa, the amounts of CO2 removed via the air space continuum would tend to be less than 10 % the CO2 production, as long as the density of roots is low (for details see next section).
The need for comprehensive data on PCO2 in waterlogged soils is amplified by further factors affecting PCO2, which make extrapolation of the data by Ponnamperuma (1984) to field soils quite uncertain. First, CO2 production is strongly dependent on organic matter (Rowell, 1988). Secondly, in rice soils, there is often some percolation, reaching 5–10 mm d–1, which would remove part of the produced CO2 (Rowell, 1988). Other percolation rates were 1–8 mm d–1 in montmorrilonitic clay at IRRI, Los Banos, as affected by different degrees of puddling and amounts of water use during puddling (Painuli et al., 1988) and 0·5–4·5 mm d–1 for six paddy soils in the Philippines (Kirk, 2004). That removal of dissolved inorganic carbon by percolation may be a major factor in limiting increases in PCO2 in the root zone is assessed for a 200-mm soil layer in a puddled rice field, by assuming that the soil is fallow, is at 30 °C and that percolation, at 5 mm d–1, would be the only cause of CO2 removal. Using the calculation given in Appendix 2c, assuming a pKa of 6·3 in the Henderson–Hasselbalch equation (caption to Fig. 2), it is assessed that a soil at 40 kPa CO2 would lose by percolation 8, 12 and 24 x 10–12 mol cm–3 s–1 at pH 6·5, 6·75 and 7·0, respectively, i.e. removal would exceed or at least be a substantial proportion of the CO2 production rates of 15–50 x 10–12 mol cm–3 s–1 assumed below in Table 3. The leaching would also slow down the increases in PCO2 with time and be more important at lower temperatures because of the higher solubility of CO2 (Table 1a). In contrast to observations for methane, ebullition would make only a small contribution to CO2 removal, because CO2 is 20 times less volatile than methane (Kirk, 2004). Thirdly, CO2 may be converted to CH4, with the redox potential for the equilibrium at –125 mV for a soil with pH of 5·0, and at –245 mV for a soil with pH of 7·0 (Rowell, 1988). In rice paddy soils in the quasi steady state, the ratio between production of CO2 and CH4 ranged between 0·28 and 0·93 (Yao et al., 1999). Nevertheless, even gas bubbles from marshland in the USA with 20–70 kPa CH4 still contained 5·5–10 kPa CO2 (Shannon et al., 1996), indicating that the bulk soil had about the same PCO2.
|
PCO2 IN ROOTS AND RHIZOMES |
|---|
When the rhizosphere is high in dissolved inorganic carbon, its uptake into root cells will be dominated by the high permeability of plant membranes to CO2, as CO2 is a weak acid and plant cells rapidly take up many weak acids in the undissociated form (Guern et al., 1991
; for CO2 see Heber et al., 1994). The presence of an undissociated acid in the medium is called an ‘acid load’ (Bown, 1985; Guern et al., 1991), as the dissociation of weak acids in the cell will tend to acidify the cytoplasm. Intensity of the ‘acid load’ imposed by exogenous total dissolved inorganic carbon in the soil solution will depend on the pH of the soil solution, as pH determines the HCO3–CO2 equilibrium (Fig. 2). This crucial point was demonstrated using carnation (Dianthus caryophyllus) callus cells; O2 uptake was stimulated two-fold by adding pure CO2 to a solution buffered at a pH of 5·7, resulting in a PCO2 of 5·5 kPa (Palet et al., 1991). Similarly, addition of HCO3–+K+ increased O2 uptake, but this stimulation decreased with increasing pHext and became negligible when pHext was 7·8, when the CO2/HCO3– ratio would be 0·03 (Palet et al., 1991). However, to conclude from these results that the effects on metabolism were due to CO2, rather than to HCO3– (Drake et al., 1997), is misleading. Whether the metabolic consequences of high PCO2 are due to the ensuing high concentrations of endogenous CO2 or to the inevitable rises in HCO3– in the cytoplasm needs further experimentation.
The only data on PCO2 in roots of plants in waterlogged soils have been published for whole root systems of Quercus nigra (water oak) and Fraxinus pennsylvanica (green ash), at 9 months after flooding to 100 mm water depth. The highest value was 10 kPa CO2 for green ash (Good and Patrick, 1987). However, this value would be an over estimate because inorganic carbon was extracted in a solution with a pH of 2·5; taking this into account, our estimates of PCO2 in these root systems, based on the data provided by Good and Patrick (1987), are between 2·8 and 5·4 kPa (for details see Appendix 4a). Obtaining reliable data on PCO2 in roots of plants in waterlogged soils is a high priority for future research.
Measurements of PCO2 in gas sampled from lacunae of rhizomes, petioles and culms of partially submerged wetland species have shown that PCO2 in these organs is at least several kPa (Table 2). Stem internodes near the soil surface of rice growing in 0·8 m of water reached 4–10 kPa CO2 (Table 2). Most of this CO2 had presumably emanated via diffusion from the roots; the only other possible source was from catabolism within the stem, as the floodwater was ruled out given that the PCO2 of the floodwater was 1·5–3 kPa when PCO2 in the internodes was 8–10 kPa (Setter et al., 1987). In this system, PCO2 in the soil will be high, so that there will be a diffusion gradient between the roots and the internodes, i.e. roots would be substantially higher in PCO2 than the internodes. Rice has no substantial convective flow (Beckett et al., 1988), so the venting of CO2 to the atmosphere via the internodes and shoots would be dependent on diffusion. Regardless, even in species with convective gas flow through their rhizomes, high PCO2 values have been observed (i.e. despite the potential of rapid ventilation); in one case PCO2 reached 10 kPa (Table 2). In the floating-leaved water lily, Nuphar luteum, in 1·2 m of water, 85 % of the CO2 flowing up the petiole was fixed by photosynthesis (Dacey and Klug, 1982a). Photosynthesis using CO2 derived from the roots is not further reviewed herein.
|
In the absence of reliable data, the value of PCO2 that may occur in roots of waterlogged plants can be speculated for two cases: (1) when PCO2 in the soil is higher than in roots, which is probably the case in soils that are waterlogged for longer than
7 d; and (2) when PCO2 in the roots is higher than in the soil, which would occur at least at the start of waterlogging. Before discussing these two cases it is relevant to discuss the possibility that root tissues in the mature zones of many wetland species may be ‘insulated’ from the soil, due to a ‘barrier’ to gas diffusion in the external cell layers, as found for O2 (Armstrong, 1979; Colmer, 2003a).
Roots with a low permeability to radial gas diffusion in basal zones
Basal zones of roots of many wetland species have a rather tight barrier to radial O2 loss (Armstrong, 1979; Colmer, 2003a), for example in rice roots at more than 20 mm from the apex (Colmer, 2003b). The key question for our theme is whether this barrier would also have a high resistance to CO2 diffusion. The layers with very low permeability to radial O2 loss are presumably associated with suberin in the exodermis. Further information on how solutes and water permeate through these layers, if at all, is scant. There are data on water permeability for rice roots, on isolated outer parts of the roots, which did contain suberin in their exodermis (Ranathunge et al., 2004). However, these data are of doubtful relevance to our theme as these roots were raised in aerated nutrient solution and therefore presumably had no strong barrier to O2 exchange. More relevant are some data for roots of Phragmites australis, which in their zone of very low permeability to O2 contained some passage areas (‘windows’) of about 1 mm in diameter, which did show significant radial O2 loss (Armstrong et al., 2000); such areas are likely to be also entry areas for water uptake. The radial O2 diffusion to the medium would be opposite to the water flow, and occur via diffusion whereas the water movement occurs via mass flow. Thus, it is reasonable to assume that when CO2 is higher in the root than in the environment (case 2, discussed below), CO2 loss to the root environment would, as for O2, be greatly restricted. By contrast, when CO2 is higher in the soil than in the root, CO2 entry into these root sections may be higher than predicted (case 1, discussed below), as fast water flows during the day may conceivably facilitate CO2 uptake by mass flow, i.e. restrictions to CO2 influx may be pronounced only at night. Such CO2 flow would be particularly prominent if water flow was through aquaporins, which may also have a high permeability for CO2 (Tyerman et al., 2002). On the other hand, if aquaporins have a low permeability to CO2, the high permeability of the lipid bilayer to CO2 would be dominant (Tyerman et al., 2002), while the effect of water flow on CO2 intake would be greatly reduced.
Case 1: PCO2 higher in the soil than in the root
Values for PCO2 that may occur in roots in waterlogged soil have been assessed using a preliminary model as described in Appendix 3a, and the predictions are shown in Table 3. These calculations also provide the diameter of the soil core from which CO2 would flow from the soil into the root. The latter is relevant to ecosystems during long-term flooding, as the wider the core from which CO2 flows to a root, the more likely it is that cores around several roots will overlap and hence gradually lower the PCO2 in the soil, owing to ventilation to the atmosphere via the gas-filled channels in the roots.
|
The preliminary model is based on the assumption that CO2 influx occurs only into the 10-mm root tip; this assumption was made for several reasons. It is the simplest model, and the predictions are particularly relevant for wetland species including rice, which, as argued earlier, might have a layer of low permeability to CO2 in the mature root zones. Furthermore, the predictions are the most conservative possible, therefore giving the minimum values of PCO2 likely to occur in roots of plants in waterlogged soils at a given PCO2 in the soil; these are the best values in a review which argues the unproven notion that roots in waterlogged–flooded soils often contain high CO2.
In Table 3, we have used an example where Dsoil is given by the relationship Dsoil/D0=0·2, where 0·2 is the product of the fractional porosity (
) and a gas-space tortuosity factor (
< 1). Results with other values of Dsoil/Do are considered after discussing the values presented in Table 3. Another assumption for Table 3 is that PCO2 in the bulk soil is 40 kPa. This value was chosen because the few data available indicate that this PCO2 would prevail in several waterlogged–flooded soils, at least for several days, so the plants need at least to survive at this particular level. Three rates of CO2 production in the soil were chosen, to evaluate the impact of this parameter on the resulting PCO2 in the root. These rates are based on the rare, but comprehensive, set of data for CO2 production in the laboratory, for 16 anaerobic rice paddy soils, from China, the Philippines and Italy, at 30 °C (Yao et al., 1999). CO2 production rates chosen were 15, 30 and 52 x 10–12 mol cm–3 soil s–1, as observed between 8 and 10 d after the start of anaerobiosis, when soil below pH 7·0 will be approaching high levels of PCO2. Subsequently, CO2 production declined and in the quasi steady state reached 0·38–5·41 x 10–12 mol cm–3 soil s–1 (calculated from Yao et al., 1999). It remains unknown whether this decline is due to feedback by the high PCO2 attained, depletion of readily decomposable organic matter or other causes.
The estimated PCO2 in the root which would be required to ventilate the CO2 influx from the soil (R(si)PCO2) to the atmosphere should be added to an estimate for PCO2 associated with ventilation of CO2 produced by the root's own catabolism (R(rc)PCO2), to obtain total PCO2 in roots (RPCO2). The minimum value for R(rc)PCO2 can be assessed by assuming a respiratory quotient of 1·0. If there were no net CO2 flux between the root and the soil, the PCO2 gradient in the gas-space continuum would be of the same magnitude as the observed PO2 gradient, but of course in the opposite direction. Any anaerobic CO2 evolution, as in ethanolic fermentation, would increase these levels of CO2.
Overall, the predictions show that the PCO2 in the root (RPCO2) generated by a combination of net influx of CO2 from the soil (R(si)PCO2) and CO2 produced by the root catabolism (R(rc)PCO2) is greatly influenced by the percentage gas-filled porosity of the roots, and to a lesser extent by root diameter and length. Surprisingly little effect arises from three-fold differences in the rate of CO2 production in the soil. The effects of different effective diffusion coefficients for CO2 in soil will be discussed after considering cases 1·1 and 1·2.
Case 1·1: predictions for roots of wetland species with high root porosity, when in flooded soil
Most of the cases given are for rice, with the gas-filled porosity in the roots set at 35 %. Furthermore, it was assumed the roots were 100 mm long and their diameter was 0·6 mm, unless stated otherwise. Predictions for various conditions are:
(1) Soil production increases of CO2 by as much as 3·5-fold only increased the predicted RPCO2 in the 10-mm root tip from 12·9 to 13·6 kPa (Table 3, columns 1–3). By contrast, the diameter of the soil core from which CO2 flows into the root is 45 % larger at the lower CO2 production rate in the soil (Table 3, columns 1 and 3).
(2) Smaller root diameters of 0·3 mm would increase RPCO2, for example in the 10-mm tip of a 100-mm-long root to 18·7 kPa compared with 13·3 kPa for a root diameter of 0·6 mm, while decreasing the predicted diameter of the soil core from which CO2 flows into the root by 20 % (Table 3, columns 2 and 4).
(3) Rice roots can reach a length of 300 mm in flooded fields (Kirk, 2003), for which RPCO2 in the 10-mm root tip would be 18·3 kPa, rather than the 13·3 kPa predicted for a 100-mm-long root (Table 3, columns 5 and 2).
(4) The conclusion in condition (3) was based on the assumption that the CO2 production rate of 300-mm-long roots would result in an R(rc)PCO2 of only 10 kPa in the 10-mm tip. However, in 300-mm-long roots, the PO2 in the 10-mm root tip is more likely to be close to zero and hence the R(rc)PCO2 at which CO2 ventilation in the gas-space continuum balances the CO2 production in catabolism is assessed at 20 kPa. Then, still assuming the bulk soil PCO2 is at 40 kPa, the RPCO2 would be 25·9 rather than 18·3 kPa (Table 3, columns 5 and 6), while the R(si)PCO2 (i.e. the component of RPCO2 due to influx from the soil) would drop from 8·3 to 5·9 kPa CO2 (Table 3, columns 5 and 6), as a result of the smaller concentration gradient between the bulk soil and the root.
(5) Because many wetland species thrive in cool climates, predictions on RPCO2 were also made for 15 vs. 30 °C. For this comparison, the lowest rate of CO2 production 15 x 10–12 mol cm–3 soil s–1 was used for the value of 15 °C, as the rate of CO2 evolution from soil has a Q10 of 2 (Yao and Conrad, 2000; Bouma et al., 1997). The predicted PCO2 in the 10-mm root tip was nearly identical at 15 and 30 °C (Table 3, column 10 vs. 3): in the soil solution a 20 % lower diffusion coefficient at 15 than at 30 °C is outweighed by the 50 % increase in solubility of CO2, while diffusion in the gas-space continuum is 10 % slower at 15 than at 30 °C (Armstrong, 1979).
Overall, these predictions for roots of rice and other wetland plants, which have in their mature zones an impermeable barrier to O2, and hence possibly to CO2 exchange, indicate that when the bulk soil PCO2 is 40 kPa, the 10-mm tips of their roots, which have no impermeable barrier to gas exchange, would reach at least 13 kPa and rise to 26 kPa PCO2 in some cases. Equally importantly, the model predicts that PCO2 in the roots of these species would remain well below the 40 kPa CO2 in the soil: the PCO2 assumed in Table 3 to be in the bulk soil.
Case 1·2: predictions for roots with porosities lower than 35 %, when in flooded soil
Gas-filled porosities in roots of several species are smaller than in rice (Justin and Armstrong, 1987; Colmer, 2003a). RPCO2 was estimated for 100-mm-long roots and the bulk soil at 40 kPa; porosities of 15 % would still limit RPCO2 to 16·5 (Fig. 5). At lower porosities, RPCO2 rises rather steeply, although even at the low porosity of 4 %, RPCO2 is still about 14 kPa below the PCO2 in the bulk soil. These lower porosities would be representative for non-wetland plants in waterlogged soil; for example, maize reaches a root porosity of 16 % (Yu et al., 1969). Importantly, as with other non-wetland species, maize lacks a barrier to O2 exchange along its roots (Darwent et al., 2003). So, the predicted RPCO2 will be substantially above the 16·5 kPa given for a root porosity of 16 % in Fig. 5, where it is assumed that only the 10-mm tip is permeable to CO2. These considerations show that roots of non-wetland species are likely to reach substantially higher internal PCO2 during waterlogging–flooding than those of wetland species. High root porosity leads to larger radii for the soil cores from which CO2 flows into the root (Table 3, columns 7–9); the amount of CO2 lost from the soil would be 1·7 times higher at a root porosity of 35 % than at 4·2 %.
|
In conclusion, when PCO2 in the soil is higher than in the roots, PCO2 in the roots can be surprisingly much lower than in the soil: depending on the PCO2 in the bulk soil and plant characteristics such as percentage gas-filled porosity, root length and resistance to CO2 movement across the external cell layers of roots, the estimated PCO2 in the roots ranged between 13 and 26 kPa. Variations in CO2 production rates in the soil have little effect on PCO2 in the roots, as these are compensated for by changes in the soil volume from which CO2 flows into the roots (Table 3, columns 1–3). Nevertheless, soil CO2 production rates remain relevant to the ecosystem of flooded fields because (1) at the start of waterlogging high rates of CO2 production will lead to rapid increases in PCO2 of the soil, and hence in roots, and (2) in the longer term the radius of the soil core from which CO2 enters roots would determine the impact that vegetation has on soil PCO2; soils with low rates of CO2 production and therefore a larger radius of soil core from which CO2 enters roots (Table 3, columns 1–3) might, when root density becomes high, intensify any gradual removal of CO2 produced in the soil via gas-space continua in the roots to the atmosphere. Let us assume that in a stand of rice, young, 100-mm-long roots would be 26 mm apart. This figure is chosen because at 40 kPa CO2 in the soil and a production rate of 15 x 10–12 mol cm–3 s–1 the cores from which CO2 flows into the root would be just touching. At this root density, the removal of CO2 to the atmosphere from a 200-mm soil layer with a PCO2 of 40 kPa would be 1·1 and 4 % of the CO2 produced at rates of 50 and 15 x 10–12 mol cm–3 s–1, respectively (protocols given in Appendix 2d). Such losses will be much lower if the PCO2 in the bulk soil has reached only 20 kPa, always assuming the same root density; for example, at 15 x 10–12 mol cm–3 s–1 the removal via the gas space continua would only be 1·6 % of the rate of production (assessed using the protocols given in Appendix 3a). These calculations are based on a simplified case; in reality, CO2 would also enter via lateral roots and the removal as a percentage of that produced by the soil would tend to increase. Nevertheless, this increase would be mitigated by the decrease in CO2 concentration gradient between the tip and the atmosphere, associated with the entry of CO2 into root sections closer to the surface.
Effect of soil porosity () and tortuosity (). There is, at present, insufficient information on the effective diffusion coefficient for CO2 in waterlogged soils. Different values of the effective diffusion coefficient (Dsoil) than the 0·2 taken in the calculations presented in Table 3 would give substantial changes in R(si)PCO2, as affected by the various characteristics of the soil and root systems; nevertheless, these changes would be only in degree, not in kind. Total porosities () range between 40 % for sands and 50 % for clays (Ahuja et al., 1999), while in some puddled rice soils can be as high as 60–70 % (Kirk, 2004). Assuming these materials are not ‘cemented’, the tortuosity factor () would be 0·66 (Penman, 1940), and similar values of 0·5–0·7 were found for the impedance factor in rice soils based on diffusion of 36Cl– (Kirk et al., 2003; the impedance factor is close to the tortuosity factor, ). Tortuosity will increase (i.e. will decrease) with decreasing soil porosity () (Kirk et al., 2003). Dsoil is derived by multiplying the product of and with D0, from the diffusion coefficient in aqueous solution. The product of and (i.e. Dsoil/D0) is 0·28 for sands, 0·33 for clays and 0·3–0·5 for the puddled rice soils. Taking the mean value of Dsoil/D0 for the puddled rice soils of 0·4, R(si)PCO2 would be 57 % higher than at a Dsoil/D0 of 0·2, and the radius of the soil core from which CO2 flows into the root would increase by 25 % (Fig. 6); nevertheless, RPCO2 would increase only from 13·3 to 15·4 kPa. By contrast, at least for the drained state, Currie (1965) has shown that crumbs (aggregates) in clays are in a ‘consolidated-cemented’ state and that these crumbs have a mean Dsoil/D0 of 0·1 (range 0·025–0·156). If these crumbs persisted following waterlogging, the pathway of CO2 diffusion may be mainly through these crumbs to root surfaces, which line these crumbs. If the Dsoil/D0 was 0·1, rather than 0·2, there would be a reduction of 42 % for R(si)PCO2 (calculated according to Appendix 3a), while the reduction in RPCO2 would be only 10 %, with a 30 % smaller radius of the soil core from which CO2 flows into the root (Fig. 6).
|
Role of HCO3– diffusion in the soil on CO2 entry into roots. This theme will only be considered qualitatively, as more precise analysis will require detailed modelling of the complex interplay between HCO3– and CO2 diffusion. Possible relevance of HCO3– diffusion depends upon both the soil and the rhizosphere pH. Assuming first that pH is uniform between the bulk soil and rhizosphere, then any HCO3– diffusion would not alter the picture derived by considering CO2 diffusion alone, as the rate constant of the uncatalysed rate of CO2 hydration is 0·037 s–1 (Raven and Newman, 1994
), i.e. much faster than the rate of diffusion prevailing in the soil. However, radial O2 loss, as occurs from root tips and laterals in many wetland plants (Armstrong, 1979; Colmer, 2003a), would complicate the picture. Radial O2 loss will tend to lower the pH of the rhizosphere, by oxidation of Fe2+ to Fe3+, which will precipitate, and by NH4+ removal, either by its uptake or by nitrification with subsequent uptake of NO3– by the roots (Begg et al., 1994; Kirk, 2004). Both oxidation of Fe2+ to insoluble Fe(III) and NH4+ removal will reduce the cation concentration in the rhizosphere and hence lower pH (Gerendas and Schurr, 1999). The Henderson–Hasselbalch equation shows that under such conditions, PCO2 would be higher in the rhizosphere than in the bulk soil, while a gradient in HCO3– towards the root surface would be equal in magnitude to the CO2 gradient from rhizosphere to bulk soil, i.e. CO2 will tend to diffuse from the rhizosphere to the bulk soil, while HCO3– would flow towards the root (Begg et al., 1994). (Note that, for convenience, this deduction has assumed an absence of CO2 uptake by the root.) Thus, the boundary conditions postulated for the model in Appendix 3a would no longer apply. Here we consider only the extreme case where the presented model would give grave errors. In Iloilo sand with rice plants, the pH at 3 d after the start of waterlogging was 5·0 at the root surface compared with 6·5 at 10 mm from the root surface (Begg et al., 1994). The Henderson–Hasselbalch equation predicts that at equilibrium, PCO2 would be 2·5 times greater at the root surface than in the bulk soil, while during CO2 uptake by the root, the diffusion of dissolved inorganic carbon to the root will presumably nearly entirely depend on the large HCO3– gradient in the direction of the root surface. Consequently, CO2 uptake by the rice roots in Iloilo sand is likely to be substantially faster than predicted by the model used in the present paper, albeit by less than expected from the high CO2 level in the rhizosphere because the diffusion of HCO3– is 40 % slower than that of CO2 (Kirk, 2004). The application of these deductions to the present model are uncertain because it is as yet unknown what the pH gradient would be around the 10-mm extending root tip. Nevertheless, substantial pH gradients might be expected despite the shorter exposure of the soil to the influence of the root, associated with the continued extension of the root tip, as this shorter exposure would be counteracted by high rates of processes tending to reduce the pH of the rhizosphere, such as vigorous uptake of NH4+ (either as the cation or as NO3– after nitrification) (see Colmer and Bloom, 1998) and oxidation of Fe2+ (Kirk, 2004), stimulated by the substantial radial O2 loss to the rhizosphere surrounding the apex (Armstrong, 1979; Colmer 2003a). Note that this complication is much less serious in better-buffered soils; for example, in Maahas soil the pH was 7·24 at 10 mm from the root and 7·1 next to the root (Kirk, 2004).
Effects of xylem flow along roots, and of convective gas-flows through aerenchyma in rhizomes. PCO2 in roots might be lower than indicated above because the CO2 efflux to the shoot may be increased due to rapid transpiration. For the xylem stream, the amount of dissolved inorganic carbon removed from the roots can be calculated using the flow rates and anatomy given by Armstrong (1979), while the amount would also depend on the pH of the xylem sap (Table 1b). In a survey of three tree species, pH of the xylem sap ranged between 5·6 and 6·5 (McGuire and Teskey, 2004). In Ricinus communis the pH of the xylem sap fluctuated between 6·0 round midnight and 5·3 at midday (Gerendas and Schurr, 1999). At pH 5·3, the ratio of HCO3–/CO2 would be 0·1; even so, substantial dissolved inorganic carbon would be removed at fast transpiration; assuming that roots had a PCO2 of 10 kPa, the xylem stream would remove 40 % of the CO2 produced in aerobic catabolism. Substantially more dissolved inorganic carbon might exit in the xylem stream if its pH was higher; for example, at pH 6·5 the HCO3–/CO2 ratio would be 1·6 (cf. equation in caption to Fig. 2), and then nearly all the CO2 produced by the root's aerobic catabolism would be removed in the xylem stream. Estimates of the same order of magnitude can be derived from transpiration ratios presented by Ludlow (1976); dissolved inorganic carbon removal was estimated to range between 20 and 100 % of production (procedures given in Appendix 2b). As the combination of CO2 production by the roots and CO2 influx from the soil may give rise to as much as 26 kPa PCO2 in the root (Table 3, column 6), much higher than the example of 10 kPa used above, substantial diurnal fluctuations in PCO2 may occur when transpiration is high during daylight hours as compared with when transpiration is low during the night.
Possible diurnal fluctuations in PCO2 in roots, as dependent on xylem flow, would be accentuated in species with convective gas flow through their rhizomes; for example, Phragmites australis has a PCO2 in its rhizomes close to 0 kPa during the day, whereas at night, when gas movement is by diffusion, PCO2 was 6 kPa (Chanton et al., 2002). Similar fluctuations for CH4 (Chanton et al., 2002) demonstrated that these diurnal changes were due to differences in gas flow, not related to photosynthesis. During darkness lasting 50 h, PCO2 in rhizomes of P. australis increased, but only in those at depths of 0–60 cm, not when the rhizomes were at greater depths in the mud (Brix, 1988). Furthermore, the deductions made here require a caveat; as discussed earlier CO2 influx into roots may become substantial during rapid water flow, and if so, the predicted fluctuations in CO2 would be dampened. Thus, the hypothesis that diurnal cycles of transpiration cause diurnal cycles in PCO2 in the rhizomes and root system needs testing; a comprehensive test would include rates of transpiration, pH of the xylem sap and convective gas flow through rhizomes, in addition to internal PCO2 measurements.