JXB Advance Access originally published online on August 13, 2004
Journal of Experimental Botany 2004 55(405):2121-2129; doi:10.1093/jxb/erh232
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RESEARCH PAPER |
Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation
School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
To whom correspondence should be addressed. Fax: +61 8 64881108. E-mail: hank{at}cyllene.uwa.edu.au
Received 14 January 2004; Accepted 18 June 2004
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Abstract |
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Roots of intact wheat plants were grown for 7–12 d in stagnant nutrient solution, containing 0.1% agar, to mimic the lack of convection in waterlogged soil. Net K+ and P uptakes by seminal and nodal roots were measured separately using a split root system. For seminal roots in stagnant solution, net uptakes as a percentage of aerated roots were between 0% and 16% for P, while K+ ranged between 15% uptake and 54% loss. For the more waterlogging-tolerant nodal roots, net uptakes in stagnant nutrient solution, as a percentage of aerated roots, were 31–73% for P and 69–115% for K+. Elongation rates of nodal roots in stagnant nutrient were about 35–43% of those for roots in aerated solution. This partial inhibition occurred in these nodal roots despite their 15% porosity (v/v). Elevation of O2 partial pressures around the shoots to 40 kPa and then to 80 kPa substantially accelerated nodal root elongation in stagnant solution, demonstrating that most of the inhibition seen with ambient O2 around the shoots was associated with a restricted O2 supply to these nodal roots. Thus, in wheat nodal roots, with a partial pressure of 20 kPa O2 around the shoots, O2 diffusion from the shoots did not completely relieve the restrictions on elongation resulting from stagnancy in the nutrient solution. These results contrast with those in the literature for rice, in which roots function efficiently in stagnant solutions (0.1% agar). So, when wheat roots are aerenchymatous there are still restrictions to O2 diffusion in the gas space continuum between the atmosphere and the functional tissues of the roots. This poor acclimation must have been due to inefficiency of the aerenchymatous axes, which may include persistence of anoxic steles, and/or restricted O2 diffusion in other parts of the gas space continuum, in either the shoots and shoot–root junction or in the root tip.
Key words: Aerenchyma, nodal roots, nutrient uptake, O2 in roots, root elongation, seminal roots, shoot O2 supply, stagnant solution, Triticum aestivum
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Waterlogging results in many changes in the soil, due to the slow diffusion of gases in solution (Armstrong, 1979
). Major changes are decreases in oxygen and increases in ethylene concentrations (Jackson and Drew, 1984), while CO2, which was 0.2–0.8 kPa in the drained soil, rose to between 5–50 kPa upon waterlogging (Ponnamperuma, 1984).
In waterlogging-intolerant plants, the consequences of waterlogging include cessation of growth, reduced nutrient concentrations of the shoots, i.e. nutrient uptake is reduced even more than growth, death of apices of the main axes of the seminal roots and, in the case of prolonged waterlogging, death of the initial root system (Jackson and Drew, 1984). The first three effects also occur for wheat in soil: for growth, Trought and Drew (1980a); for nutrients, Trought and Drew (1980b). These responses can be reproduced with wheat in anaerobic nutrient solutions bubbled with N2 gas (Trought and Drew, 1980c), indicating that the absence of O2 in the waterlogged soil may be, at least partly, responsible for these adverse effects. The differences in tolerance of seminal and nodal roots of wheat were associated with development of a higher porosity in the nodal but not in the seminal roots and the concomitant ability to conduct more oxygen from the shoot to the root (Trought and Drew, 1980c; Barrett-Lennard et al., 1988).
Experiments with N2-flushed nutrient solutions have contributed much to knowledge of the response of plants to low O2 in the root medium. However, these N2-flushed solutions often contain some O2 (Kuiper et al., 1994), so they do not quite simulate the response to the lengthy waterlogging of soil when the soil becomes anoxic. Low, but not zero, O2 concentrations in soil occur in a number of ecological situations; such as before the O2 in the soil is depleted at the start of waterlogging and when the soil has a low gas-filled porosity, either during the first days after the water table recedes, or permanently in compacted soils (Drew, 1992).
There are two further problems using N2 flushing of solutions to mimic plant response to waterlogged soils. Firstly, the continuous removal of ethylene may reduce aerenchyma formation, which, in turn, may limit O2 supply to the root and hence nutrient uptake. Consistently, the percentage porosity (v/v) of nodal roots of wheat grown in stagnant solution was 15%, compared with values in N2-flushed solutions of 2.5% (Wiengweera et al., 1997) and 11–12% (calculated for the whole root from values for sections in Barrett-Lennard et al., 1988; Thomson et al., 1990).
Secondly, N2 bubbling will ‘strip’ O2 from the root surface, leaving only a very thin, unstirred, layer around the epidermis. By contrast, in stagnant media, radial O2 loss from the root may lead to a build-up of O2 in the rhizosphere. Thus the removal of O2 by N2 flushing may reduce both nutrient uptake by the roots and the O2 reaching the elongating root tips.
The lack of convection in waterlogged soil can be mimicked using a 0.1% stagnant agar nutrient solution culture (hereafter called: stagnant solution). The response of wheat in this medium in terms of growth, and nutrition of the plant as a whole, was described earlier (Wiengweera et al., 1997).
The novel aspects addressed in the present paper are: (i) The extent to which, in a stagnant medium, nutrient uptake by the plant occurred via seminal and nodal roots, respectively. This was achieved using a split root system and then measuring the depletion of potassium and phosphate in the stagnant nutrient solutions. (ii) Whether the aerenchymatous nodal roots of wheat, grown in stagnant media, receive sufficient O2 for optimal elongation. Therefore, their elongation was measured while surrounding the shoots with elevated partial pressures of O2 between 40–80 kPa. In earlier experiments, elevating the O2 partial pressure around the shoots stimulated elongation of seminal wheat roots, which had been grown since germination in solution without forced turbulence, even though these roots had 12% porosity (Thomson et al., 1990). However, these findings do not exclude a better O2 supply to nodal roots; these may have a different structure, or acclimate better in stagnant solutions than in solutions without forced turbulence.
As an alternative to an insufficient O2 supply, the elongation of roots in stagnant nutrient solutions might be reduced by a failure of the aerenchyma to vent sufficient ethylene, or CO2, from the roots to the atmosphere. Whether these factors can be ruled out conclusively when elevated O2 pressures around the shoots improve the rate of root elongation will be considered in the Discussion.
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Materials and methods |
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The methods as described by Wiengweera et al. (1997)
will not be repeated here, except for some key information.
Raising of seedlings
Intact wheat seedlings (Triticum aestivum cv. Gamenya) were used in all experiments. On the 4th day after germination seedlings were transferred from a darkroom at 20 °C to a phytotron under natural light between 1000 and 2000 µmol m–2 s–1 and 20/15 °C day/night temperatures. On day 7, the roots of the seedlings were transferred to aerated nutrient solution (complete composition in Wiengweera et al., 1997), this nutrient included in mol m–3: 6.5 K+ and 0.64 
with a pH of 6.5.
To dissolve the agar (0.1%, w/v), all solutions were autoclaved at 120 °C and 400 kPa pressure for 15 min and then cooled overnight to room temperature. High quality agar was essential and was purchased from Agar-BACTO-AGAR: ‘Difco’ certified, Difco Laboratories, Detroit, Michigan, USA.
Measurement of K+ and P uptake by seminal and nodal roots (experiment 1)
Sixteen-day-old seedlings were transferred to clear plastic pots, wrapped in black plastic sheets, with two compartments, each of 500 ml, containing either stagnant nutrient (agar at 0.1%, w/v), or aerated nutrient without agar. Seminal and nodal roots were in separate compartments.
P and K+ uptake were measured by changes in concentrations in the nutrient solution. However, during reaeration there was only the analysis of P, not of K+. Decreases in K+ never exceeded 15% of the initial concentration and accuracy was achieved by at least three separate dilutions for each sampling. P depletion in the aerated solutions reached 40%. However, the reduction to 0.38 mol m–3 would not have affected the results since net P uptake was similar over the range 0.16–0.64 mol m–3 P (Wiengweera et al., 1997). All nutrient solutions were sampled after stirring the agar solution for 30 s and then renewed.
There were three plants per pot and six replicates for each treatment during the 12 d exposure to stagnant nutrient solution. Subsequently, three replicates were harvested; leaving the other three replicates to be evaluated after the roots of the stagnant nutrient had been transferred to aerated solutions.
Response of elongation of nodal roots to elevated O2 partial pressures around the shoot (experiments 2 and 3)
Roots of 16-d-old wheat seedlings were either transferred to grow in stagnant nutrient solution for 7 d, or were grown continuously in aerated solution. When the seedlings were 23-d-old their roots were transferred to clear plastic pots. At this stage the new nutrient (with 0.1% agar) was first bubbled with N2 gas, to match the very low O2 concentration present after 7 d of exposure to stagnant solution (Wiengweera et al., 1997). The shoots were then enclosed in a clear plastic vessel, which had an inlet and outlet through which the gas mixture of the desired partial pressure of O2 flowed around the shoots. The experiments were in the natural light of the phytotron; however, while the shoots were in the vessels photosynthesis would have been slight due to the very low CO2 supply. To maintain humidity around the shoot, a piece of moistened filter paper was placed in the vessel. Elongation of roots of 1–2 cm, 5–6 cm, and 11–12 cm was measured every hour using vernier microscopes.
Analytical techniques
Determination of P in the nutrient solution: Because of the presence of agar, the solutions for P were evaporated and then dry-ashed after the addition of Mg(NO3)2.6H2O, with subsequent dissolving in dilute HCl. P in these digests was determined by absorbency of molybdovanadophosphate at 820 nm.
Determination of K+ in the nutrient solution: Nutrient solutions were diluted 10-fold (v/v) with a solution containing 500 µg ml–1 CsCl and K+ concentrations in these solutions was determined by atomic absorption spectrophotometry (Perkin-Elmer, AA 5000).
Calculations of rates of growth and of net nutrient uptake
Relative growth rate (RGR) of the roots was calculated using the equation:
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Net rates of ion uptake (K+ and P) were calculated based on the depletion of ions from the solutions by:
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This is a modification of the equation by Pitman (1976), since changes in ion concentrations in the solution were measured instead of the ion content of the plant. In this modified equation M denotes the ion content of the solution.
Assessing the dry weight of roots: Since no dry weights of the roots were obtained at days 4 and 8, these were estimated from the relative growth rate and the dry weight at the start of the experimental period using the equation:
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RGR was for the 12 d of treatment, W is dry weight, and t1 and t2 the times for which dry weight has to be assessed.
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Results |
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Growth, K+ and P uptake by seminal and nodal roots (experiment 1)
Growth: Growth data are not presented in detail. The growth response of the roots of these intact wheat plants was similar to that recorded in the literature for N2 bubbled solution culture (Trought and Drew, 1980c
; Barrett-Lennard et al., 1988). In stagnant solutions, seminal roots ceased dry weight increments, while nodal roots had the same relative growth rate of 0.33 d–1 (dry weight basis) as in the aerated nutrient (Wiengweera, 1994). The number of primary axes of nodal roots were 11 for the stagnant nutrient solution and 8 for the aerated nutrient (Wiengweera, 1994), however, the mean length of the roots was 30% shorter in the stagnant nutrient, so that the total nodal root length was similar in the two treatments.
P and K+ uptake: For seminal roots in stagnant nutrient solutions, rates of net P and K+ uptake were severely reduced and there was even net loss of K+ between 8–12 d (Table 1). There were no clear time trends for net P uptake (Table 1a), but K+ showed some net uptake during the first 8 d and then a marked net loss between 8 d and 12 d after transfer from aerated to stagnant nutrient (Table 1). The net K+ loss may not apply to the entire seminal root system, since heavy losses in the tip regions (Greenway et al., 1992) might have masked uptake in the more basal tissues, which would have received some O2 from the shoot. After the return from stagnant to aerated nutrient solutions, net P uptake increased 1.7-fold above the rates in continuously aerated solution (Table 1b).
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In nodal roots exposed to stagnant nutrient, net P uptake was reduced below that of aerated roots throughout the experimental period (Table 1a), while net K+ uptake was reduced only during the first 8 d (Table 1c). Between 4 d and 8 d, net rates of P and K+ uptake were reduced by about 30%, relative to uptake by aerated nodal roots. Between 8 d and 12 d, net P uptake was reduced by 70%, while net K+ uptake was similar for stagnant and aerated nodal roots. This relief of the degree of inhibition with time, in net K+ uptake by the roots in the stagnant solution, were due to decreases with time in rates of net K+ uptake by the roots in aerated solutions. In the roots in stagnant nutrient solution, rates of net K+ uptake expressed as mmol g–1 root DW d–1 did not change with time (Table 1c). After the return from stagnant to aerated nutrient solution, net P uptake by nodal roots increased to the same rate as the uptake in continuously aerated solution (Table 1b).
Response of elongation by nodal roots to elevated partial pressures of O2 around the shoot (experiment 2)
Roots grown in stagnant nutrient solution (experiment 2): The elongation rates at 21 kPa O2 around the shoots was fastest in the 5–6 cm long roots, intermediate in the 1–2 cm long roots, and slowest in the 11–12 cm long roots (Table 2). All these roots increased in elongation when the partial pressure of O2 around the shoots was elevated from 21 to 42 kPa, with further increases when the partial pressure of O2 was elevated from 42 to 84 kPa (Table 2). Increases in elongation at 84 kPa relative to 21 kPa were 2-fold for 1–2 and 5–6 cm roots and 5-fold for 11–12 cm roots. The large increase in elongation of the longer roots being associated with their slow initial elongation rate at ambient O2 around the shoots (Table 2). Upon lowering the partial pressure of O2 around the shoots, from 84 to 21 kPa, elongation rates of the roots declined. Between 2–4 h these rates reached the initial rates at 21 kPa for 1–2 cm and 5–6 cm roots, while the 11–12 cm roots, although decreasing, still elongated 2.5 times faster than at the start of the experiment (Table 2). Presumably, relatively high O2 concentrations in the rhizosphere of roots in stagnant nutrient, due to high radial O2 loss during the period the O2 around the shoots was elevated, persisted for some time after lowering the partial pressure of O2 around the shoots from 84 kPa to 21 kPa.
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Comparison between roots grown in stagnant and in aerated nutrient solution (experiment 3): Roots grown in stagnant nutrient solution responded similarly to those in experiment 2 (cf. Table 3 with Table 2). However, the decrease in elongation upon lowering the partial pressure of O2 around the shoots from 42 kPa to 21 kPa was already complete during the first 2 h (Table 3). This discrepancy between experiments 2 and 3 was presumably related to the 2 hourly replacement with fresh N2-bubbled agar in experiment 3, i.e. replaced each time when the partial pressures of O2 around the shoots were changed. Thus, when transferred from 42 kPa to 21 kPa, there was no residual effect of a build-up of O2 in the stagnant nutrient solution, which otherwise would occur due to the increased radial O2 loss as a result of high partial pressure of O2 around the shoots.
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Continuously aerated roots elongated more than twice as fast as roots in stagnant nutrient solution (Table 3), even so, the 10–12 cm long, aerated roots elongated at only half the rate of the 3–4 cm long roots. These differences between long and short roots were abolished by increasing the oxygen partial pressures around the shoot from 21 kPa to 48 kPa; the elongation rate of the 10–12 cm long roots was more than doubled, but the elongation rate of short roots remained unaltered (Table 3). This response is consistent with a critical O2 pressure of 30 kPa, for respiration of excised maize root tips (Saglio et al., 1984
). These critical O2 pressures for exogenous O2 supply depend on root diameter and respiration rates (Armstrong et al., 1991). So, in tips of nodal roots of wheat there might still be, at least some, O2 deficiency when in aerated solutions. If so, supplementary O2 diffusion from the shoot via the normal non-aerenchymatous intercellular spaces of the cortex, may be inadequate since the porosity of these non-aerenchymatous roots is only 5% (Wiengeera et al., 1997).
Possible adverse effects of high partial pressures of O2 around the shoots
In the present experiment there was no evidence for adverse effects of either the high partial pressures of O2 around the shoots, or the low CO2 supply during the period O2 was elevated, even though these treatments give the danger of increased production of free O2 radicals. This conclusion is based on the following evidence. Firstly, the elongation of nodal roots increased rather than decreased when the O2 pressure around the shoots was elevated, even when the O2 pressure around the shoots was increased from 42 kPa to 84 kPa (Table 2). Furthermore, when O2 around the shoots was decreased again from 84 kPa to 21 kPa, the rate of elongation did not decline further than the values for plants with shoots continuously at 21 kPa O2 (Tables 2, 3), i.e. there was no permanent injury. Secondly, at the end of the experiment there was no visible injury in the shoots which had been at the high partial O2 pressures of 42–84 kPa for 4 h.
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Discussion |
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This paper demonstrates that, in wheat grown in stagnant nutrient solutions, there are both severe adverse effects on seminal roots and below-optimum performance of the aerenchymatous, nodal roots. In this discussion these responses are compared with results in the literature on rice, which thrives on flooded soils.
Evaluation of performance of seminal and nodal roots
Nutrient uptake: The data obtained with the split root system in stagnant nutrient solution, showed that the well-known reduction of nutrient uptake by wheat in waterlogged soils (cf. Introduction) is due to a combination of a near cessation of uptake by seminal roots, and a suboptimal uptake by nodal roots. Despite these poor performances, the roots were not severely injured as shown by the recovery of net P uptake when reaerated. Such a performance, well below capacity during exposure to O2-deficient media, was shown even more clearly by measuring the net uptake during the first 23 h after transfer from 0.003 to 0.27 mol m–3 O2; during this period the rates of net K+ uptake of both nodal and seminal roots was about 3-fold faster than in continuously aerated roots (Kuiper et al., 1994). The high net uptake of nutrients after a return to air is presumably associated with the shoot concentrations, which were 50% lower for K+ and 60% lower for P than in aerated plants (Wiengweera et al., 1997). The stimulation of uptake in plants with low endogenous concentrations was demonstrated for aerated wheat roots; when only one seminal root received P, this root took up P twice as fast as when the whole root system received P (Drew and Saker, 1986).
Seminal roots: The nutrient uptake by seminal roots in stagnant solution was much lower than for the same wheat cultivar when grown in N2-bubbled nutrient solutions at 0.003 mol m–3 O2; when rates of net uptake on a fresh weight basis were at 25–80% of aerated rates for 
and K+ (Kuiper et al., 1994). This difference is presumably due to the low but continuous O2 supply from the contaminant of O2 in the industrial N2 gas: provided there is rapid bubbling the 0.003 mol m–3 O2 may still sustain up to 10–35% of the respiration rates of aerated roots (Kuiper et al., 1994). By contrast, the lack of convection in stagnant solution would prevent any O2 supply from the medium to the root surface, while the low porosity of 3% in the seminal roots (Wiengweera et al., 1997) will only provide a very restricted O2 supply from the shoots (Armstrong, 1979).
Nodal roots: Nutrient uptake from stagnant nutrient solutions, albeit better than in seminal roots, usually remained below that in aerated solution. Similarly, in N2-bubbled solution, below-optimum functioning of nodal roots of wheat was indicated by the lower selectivity of uptake of K+ over Na+ than in aerated roots (Buwalda et al., 1988). There are strong arguments, which favour the notion that in aerenchymatous, nodal roots of wheat, O2 supply from the shoots is still insufficient to achieve optimum functioning, despite a porosity of 15% in the roots as a whole. These arguments will be given in the later section on causes for the inefficient functioning of nodal roots.
Alternative explanations to limited O2 availability would be: (i) The death of cortical cells due to aerenchyma formation. However, this is unlikely since P uptake was similar in reaerated, previously stagnant, roots and in continuously aerated roots (Table 1b) and this is consistent with high nutrient uptake by aerated, aerenchymatous maize roots (Drew and Saker, 1984). (ii) High concentrations of ethylene or CO2 inhibited nutrient uptake. This possibility cannot be excluded since in maize roots 5 µl l–1 ethylene for 14 d reduced P concentrations in the shoots of maize by about 30% (Jackson et al., 1981). (iii) Diffusion limitation of nutrients to the root surface uptake due to the lack of convection in the nutrient solution, however, these were ruled out by using high exogenous nutrient concentrations in the bulk solution (see Introduction).
These inhibitions of nutrients by wheat roots contrast with the results for rice, which had high rates of nutrient uptake in N2-bubbled solutions (John et al., 1974). Consistently, the net N uptake of rice roots in stagnant agar solution over 18 d was, at most, 10% lower than in aerated solutions (Rubinigg et al., 2002).
Elongation
The large stimulatory effect on the elongation of nodal roots in stagnant nutrient solution by the elevation of the partial pressure of O2 around the shoots, demonstrates that, at ambient O2 in the air, the gas space continuum still does not provide sufficient O2 for optimal functioning. By contrast, 50–70 mm long nodal roots of rice were only reduced in elongation when the O2 around the shoot was reduced below 5 kPa (Armstrong and Webb, 1985). Thus the gas space continuum is presumably more efficient in rice than in wheat. However, this conclusion remains somewhat equivocal, since the rice roots of Armstrong and Webb were at 23 °C, which is suboptimal for rice. Consistently, the maximum elongation of the rice roots was 0.33–0.63 mm h–1 (Armstrong and Webb, 1985), compared with 1.1 mm h–1 for the 5–6 cm long nodal wheat roots (Table 2). Nevertheless, an elongation rate of rice of 1.1 mm h–1 would presumably be reached at about 10 kPa O2 around the shoot, i.e. 4–8 times lower than for wheat (cf. Table 2).
It was surprising that even the very short, 1–2 cm roots of wheat elongated much faster during increased O2 supply from the shoots. Diffusion models predict that the elongation of individual roots will cease only when the diffusion path between the shoot–root junction and the terminal apex reaches a certain length, as set by the demands and the resistances of the gas space continuum (Armstrong, 1979). Furthermore, in stagnant nutrient solution wheat nodal roots reached the maximum length of 140 mm, as predicted by the Armstrong model (Watkin et al., 1998). The possible explanations for the substantial reduction in elongation of the short roots include: (i) elongation is slowed well before ceasing altogether; (ii) roots of different lengths have different structures and volumes of aerenchyma and diffusion paths to the apex. This remains possible, since aerenchyma-porosity was not measured for roots of different lengths; and (iii) decreases in ethylene production at higher O2 concentrations, as shown for maize by Jackson et al. (1984). However, the inhibitor of C2H4 action (DIHB) did not improve the elongation of maize roots at low exogenous O2, so Jackson et al. (1984) concluded that ethylene was not involved in the observed reduction of elongation. This conclusion still needs to be verified for wheat in stagnant solutions.
Causes of inefficient performance of wheat exposed to stagnant solutions despite formation of aerenchymatous nodal roots
The stimulation of elongation by the elevation of partial O2 pressure around the shoot demonstrates that, at ambient O2 pressures around the shoots, the O2 flux through the gas space continuum from the shoots to nodal roots of wheat is inadequate to achieve their optimal functioning, despite their 15% porosity and as much as 22% aerenchyma at 50 mm behind the apex (Wiengweera et al., 1997). Restrictions in O2 supply can be associated with the percentage and structure of the aerenchyma and radial loss to the root environment, or with the configuration of the packing of the living cells which can be either hexagonal or cubic; with a 2-fold lower porosity in the hexagonal than in the cubic configuration over the full range of closeness of packing (Justin and Armstrong, 1987). The configuration is cubic in rice (Justin and Armstrong, 1987), but hexagonal in wheat as shown in electron micrographs (Huang et al., 1994) and by microscopic observations for the present wheat cultivar in stagnant solutions (ELJ Watkin and H Greenway, unpublished data).
Longitudinally, there are three possible locations at which O2 diffusion to the root tip can be restricted. (i) High resistances to gas flow in the gas spaces in the leaves and the root–shoot junction. These gas spaces are well developed in many wetland plants including rice (Armstrong and Drew, 2002; Armstrong et al., 1994a), but whether this part of the gas–space continuum has the same efficiency in non-wetland plants is unknown. Furthermore, the coleoptile sheath in young wheat seedlings limited O2 entry into the shoot (Thomson and Armstrong, 1990), and, possibly, this also applies to the sheaths of leaves. (ii) Wheat roots do not form a barrier to radial O2 loss in the epidermis-hypodermis, as shown by increasing radial O2 loss from the tip towards the root–shoot junction (Barrett-Lennard et al., 1988; Thomson et al., 1990). This contrasts with rice roots grown in either waterlogged soil or in stagnant nutrient solution, which have a barrier to O2 loss over substantial lengths of their axes, presumably leaving more O2 available to the stele and apex (Armstrong, 1971; Colmer et al., 1998). Furthermore, the lack of the barrier would tend to reduce the O2 concentration in the aerenchyma.
Nutrient uptake at the epidermis may not be the first to be affected at low endogenous O2, since O2 concentrations at the epidermis of nodal roots of wheat were still 1–2 kPa at the root tip and 1.5–2.5 kPa at 40 mm behind the tip (Barrett-Lennard et al., 1998). More likely, anoxic cores may develop in the stele, as indicated for maize roots by models (Armstrong and Beckett, 1987), O2 microelectrodes (Armstrong et al., 1994b), and metabolic evidence (Thomson and Greenway, 1991). Such anoxic cores are particularly likely in wheat roots since the stele comprises 18–20% of the cross-sectional area of the root (from electron micrographs of Huang et al., 1994); this compares with a value of less than 5% for nodal roots of rice (Colmer, 2003). Wide steles would tend to have a high O2 demand and would therefore become anoxic at higher O2 in the adjoining cortex than narrow steles (Armstrong and Drew, 2002). Consistently, in maize roots, which have a wide stele, Cl– flux to the xylem was reduced by 40% when the cortex still received sufficient O2 for oxidative phosphorylation, while part of the stele was anoxic (Gibbs et al., 1998).
(iii) In the root tip, the aerenchyma ends in both rice and wheat at 20 mm from the root tip (rice, Armstrong, 1971; wheat, Thomson et al., 1992). However, in wheat roots, with their hexagonal configuration, the resistance to O2 diffusion would be higher than in rice, where the cubic configuration results in a non-tortuous pathway with 9% porosity, ending a few cells distance from the root cap (Armstrong, 1979). This difference would be important, not only for elongation but also for nutrient uptake, particularly because the tips would contribute a rather large amount of the total roots in the rather nodal short roots in the present experiment.
For the plant as a whole, the volume of functional rather than total root system would also be of key importance. Since this paper shows that the seminal root system of cv. Gamenya in stagnant solution absorbs negligible nutrients, the rather small volume of nodal roots has to supply the entire shoot demand. Quantitatively, the ratio of fresh weight of functional root to shoot after 14 d of treatment was 0.20 for the stagnant solution (nodal roots/shoots) and 0.60 (total root/shoot) for aerated solution (Watkin et al., 1998). Similarly, in soil, these ratios were 0.52 and 1.23 for waterlogged and drained conditions, respectively (Thomson et al., 1992). So, even if the individual nodal wheat roots would be more efficient in ion uptake than found in this paper, their total volume remains small relative to the volume of the functional root system (i.e. the seminal+nodal roots) in drained soil. Hence these nodal roots are unlikely to be able to provide sufficient mineral nutrients for the rapid growth of the shoots. Such results reinforce the importance of a large number of nodal roots and/or aerenchyma development in seminal roots. Seminal roots of two winter wheat cultivars grown for 14 d in drained sand and then submitted to waterlogging developed aerenchyma; in the most prominent case (cv. Savannah) aerenchyma as the percentage of the cortical area was 12% at 1 cm from the tip and between 21–28% at 30 cm or further from the tip (Huang et al., 1994). Similarly, two wild relatives of wheat from wetlands increased in seminal root porosity from 3.4% to 7.4% after they were grown for 21 d in stagnant nutrient solution (McDonald et al., 2001). By contrast, in cv. Gamenya, porosity in seminal roots developed only when grown in solutions without forced turbulence since germination (Thomson et al., 1992). Whether these differences between the wheat cultivars is genetic, or due to the experimental conditions, needs to be established.
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Concluding remarks |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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The current results on nodal root elongation prove the usefulness of a combination of stagnant solution and elevation of O2 around the shoots, to elucidate further the efficiency of the gas-space continuum to provide sufficient O2 for optimal functioning of the roots. For wheat, this technique would confirm the present hypothesis that, at ambient O2 around the shoots, O2 supply remains insufficient for optimum nutrient uptake, even in the aerenchymatous nodal roots. Similarly, the efficiency of the gas space continuum in seminal roots of the cultivars which do form aerenchyma deserves evaluation. This is particularly important in view of the key ecological importance of seminal roots in a species that has a predominance of seminal roots.
For rice, confirmation is needed that the O2 supply from the shoots is sufficient for the optimum elongation of roots that have not reached their maximum length. Of at least equal interest is the response of nutrient uptake, even though there is little doubt that the net nutrient uptake of roots of paddy rice is adequate, as shown by its high yields in flooded soils (Peng et al., 1999). Nevertheless, elevation of O2 around the shoot would elucidate the mechanisms by which this optimum uptake is achieved. For example, an inadequate O2 supply for optimum uptake may be offset by increases in the capacity for nutrient uptake (John et al., 1974).
Finally, the inefficiency of the gas space continuum in nodal wheat roots is relevant to understanding the responses to waterlogging in the field. The inefficiency would presumably be aggravated in soil, which often presents a large sink for O2, so then wheat roots would be further disadvantaged compared with rice due to their lack of a barrier to radial O2 loss.
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Acknowledgements |
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Amara Wiengweera received a grant from Ausaid. Tim Colmer and Bill Armstrong for incisive criticisms on several drafts, including the final one. Mike Jackson, Eddy Barrett-Lennard, and Imran Malik also commented on a draft. We also thank the ecophysiology discussion group of the School of Plant Biology for critical comments.
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Footnotes |
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* Present address: Department of Agriculture of Thailand, Bangkhen, Bangkok Thailand.
Definition: Stagnant solution, when convection is prevented by adding 0.1% agar. Conventional stagnant solutions are referred to as solutions without forced turbulence.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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