Abstract
The responses of root aerobic respiration to hypoxia in three common Typha species were examined. Typha latifolia L., T. orientalis Presl, and T. angustifolia L. were hydroponically cultivated under both aerobic and hypoxic growth conditions to measure root oxygen consumption rates. Hypoxia significantly enhanced the root aerobic respiration capacity of the two deep-water species, T. orientalis and T. angustifolia, while it did not affect that of the shallow-water species, T. latifolia. T. angustifolia increased its root porosity and root mass ratio, while T. latifolia increased its root diameter under the hypoxic growth conditions. The relative growth rates in biomass of T. orientalis and T. angustifolia were 59 and 39% higher, respectively, under the hypoxic growth conditions than under the aerobic growth conditions. In contrast, that of T. latifolia did not differ between the two conditions. In T. orientalis and T. angustifolia, enhanced root aerobic respiration rates under the hypoxic growth conditions would have increased the nutrient uptake, and thus higher relative growth rates were obtained. For the deep-water species, T. orientalis and T. angustifolia, the root aerobic respiration capacity was enhanced, probably in order to maintain the generation of respiratory energy under hypoxia.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Wetland plants usually root in waterlogged soil, where the oxygen concentration around the root tissue is nearly zero, due to the substantial consumption of oxygen in chemical and biological oxidation processes (Teal and Kanwisher 1966; DeLanune et al. 1990; Lorenzen et al. 1998). The roots thus always experience oxygen deficiency and anoxic stress (Jackson and Armstrong 1999). Wetland plants widely differ in their abilities to tolerate the anoxic stress, which induces zonal distribution based on water depth (Yamasaki 1984; Grace 1989; Brix et al. 1992; Weisner et al. 1993). Elucidating the differences in morphological and physiological strategies to overcome anoxia in wetland plants would thus greatly help us to understand wetland ecosystems more precisely.
When deprived of oxygen, in flooding, plant cells convert from aerobic to anaerobic metabolism. Anaerobic metabolism is considered to be an adaptation to anoxia since it allows ATP production to continue, although usually at a much lower rate than under aerobic respiration (Cronk and Fennessy 2001). In wetland plants, oxygen is soon re-introduced by elongation of stems or petioles to reach the water surface or by development of other oxygen-carrying structures; subsequently, the plant cells convert to aerobic respiration (Cronk and Fennessy 2001). Even beyond critical situations where they are inundated, many wetland plants develop aerenchymatous lacunae that serve as a pathway for oxygen transport from aboveground parts to underground parts in order to overcome the anoxic problem (Teal and Kanwisher 1966; Armstrong 1972; Justin and Armstrong 1987). Oxygen in leaves can move downward by diffusion with low resistance through the lacunae to support aerobic respiration of the roots. Some species have another mechanism to transport a massive amount of oxygen to their underground parts. They supply oxygen by through-flow convection driven by pressure differentials (Dacey 1980, 1981; Armstrong and Armstrong 1990; Brix et al. 1992; Grosse 1996). In addition to their own respiratory consumption, the oxygen molecules are partly released to surrounding soils and form an oxidative layer around the root surfaces, which prevents excessive plant absorption of toxic reduced substrates such as Fe2+, Mn2+ and sulphide (Armstrong 1967; Mendelssohn and Postek 1982; Sorrell and Dromgoole 1987; Armstrong et al. 1992; Sorrell and Armstrong 1994).
In addition to oxygen supply to roots and radial oxygen loss from root surfaces to surrounding soils, root respiration is also an important physiological process that helps to ameliorate the ill effects of flooding. It is well known as an aspect of the homeostasis of respiration that some plants have the ability to maintain similar respiratory rates (measured at the growth temperature), even when grown at different temperatures (Lambers et al. 1998; Kurimoto et al. 2004). In addition to responding to temperature differences, respiration homeostasis can also operate in response to differences in the growth oxygen conditions: the root respiration rate of the flooding-tolerant Carex pseudocyperus L. increased when it was grown in a hypoxic solution compared with an aerated solution (Moog and Brüggemann 1998), while there was no apparent difference in root respiration rate for the flooding-sensitive C. extensa Goodenough (Moog and Brüggemann 1998) or for various species of terrestrial herbs (Mark et al. 2001). Increased root respiration in hypoxia could be the case among many flooding-tolerant plants although it has been little demonstrated. In order to obtain a deeper insight into the mechanisms for overcoming hypoxic stresses, more precise information on acclimation in root respiration is required.
A hypothesis was made that plant species growing in deep-water regions, which are more likely to be flooding-tolerant species, increase their root aerobic respiration capacity to a greater extent than species growing in shallow-water regions, in order to maintain the generation of respiratory energy under hypoxia. To confirm this, we conducted an experiment using three Typha species differing in distribution with regard to water depth: Typha latifolia L., distributed in shallow-water regions, and T. orientalis Presl and T. angustifolia L., distributed in deep-water regions. T. latifolia and T. angustifolia are distributed throughout the world and the difference in their habitat based on water-depth gradient has been well demonstrated (Grace and Wetzel 1982; Grace 1988, 1989). For T. orientalis, however, there have only been a few studies, probably because its distribution is restricted to eastern parts of Asia and Oceania. Sorrell et al. (2000) reported that T. orientalis was distributed in areas of up to 150 cm in water depth. A similar distribution pattern was observed at the Ushigafuchi Pond in Tokyo, Japan, where the three Typha species co-occur along the water depth gradient (T. Matsui, in preparation).
Typha species are macrophytes possessing an efficient convective through-flow mechanism (Brix et al. 1992). Many investigations have been made on the differences in their abilities to supply oxygen to roots, and these have proved that T. orientalis and T. angustifolia are superior in their capability for through-flow convection to T. latifolia (Brix et al. 1992; Bendix et al. 1994; Tornbjerg et al. 1994; White and Ganf 1998; Sorrell et al. 2000; Sorrell and Brix 2003). Here, we compare the responses among the three Typha species to rhizosphere hypoxia, particularly in root aerobic respiration rate, as well as in growth characteristics and root morphology.
Materials and methods
Plant materials and experimental design
Seeds of Typha species were collected from fallow fields in Chiba City, Japan, in November 2002. The following April, the seeds were sown and germinated in sediments in a plastic tray in a greenhouse at Chiba University and watered daily to maintain the sediments in a water-saturated condition. Seedlings grown to 3 cm in shoot height were established in separate pots (540 ml) containing 300 ml of sediments, which were collected from Lake Inba-numa, 20 km north of Chiba City, in March 2003. The plants were cultured for 7 weeks in the open air and watered daily before being used for the greenhouse experiment. Thirty healthy and uniform plants of each species were transplanted to hydroponic chambers. In the greenhouse, the plants were precultured further for 4 weeks under full sunlight at 27–34°C air temperature with 25%-strength Hoagland’s solution, which was renewed every 2 days.
We prepared two growth conditions: aerobic (0.19 mmol O2 l−1) and hypoxic (0.02 mmol O2 l−1). For each species, four plants were randomly selected and transplanted to a hydroponic tank of each growth condition after measuring their fresh weight. In order to estimate their initial dry weight, the fresh weights of another ten plants were recorded, and they were then oven-dried for 72 h at 80°C to obtain the dry weight. To maintain the nutrient solution at aerobic (0.19 mmol O2 l−1) and hypoxic (0.02 mmol O2 l−1) conditions, atmospheric air and oxygen-free nitrogen gas, respectively, were continuously introduced. The oxygen concentration of the nutrient solution was monitored by a Clark-type oxygen electrode sensor (HDO-110; Denki Kagaku Keiki, Tokyo) throughout the experimental period. The solution was circulated by a pump throughout the experimental period and renewed every day in order to maintain a stable nutrient condition. The shoot heights and numbers of leaves of all the plants were measured every 6 days. The experiment was run for 40 days.
At the end of the experiment, the roots were used for measurements of root aerobic respiration rate and root morphology, as described below. After the measurements, the dry weights of roots and the remaining aboveground parts were measured after oven-drying for 72 h at 80°C.
Root aerobic respiration
The detached root was submerged in a 200-ml flask filled with oxygen-saturated water in the dark. The ambient water temperature was maintained at 20°C throughout the measurements. The decrease in dissolved oxygen concentration was continuously monitored until it reached 0.003 mmol O2 l−1 measured by a Clark-type oxygen electrode sensor (UD-101E; Central Science, Tokyo) mounted through the central hole of the rubber stopper of the flask. The water was vigorously stirred by a Teflon-coated magnetic stir bar at the bottom of the flask. The procedure was repeated 3 times for each plant sample. The root oxygen consumption rate (nmol O2 g−1 root dry weight s−1) was estimated as the decrease in the amount of dissolved oxygen in the flask.
Root porosity and diameter
After the respiration measurement, the porosity of root (POR) in percent was determined by the pycnometer method (Jensen et al. 1969). An approximately 0.2-g segment of undamaged root was employed for the measurement. First, a 25-ml pycnometer was filled with water and weighed (p). The root sample was gently blotted dry on filter paper and weighed (r). The root sample was submerged in the water in the pycnometer and weighed (pr). The root sample was retrieved from the pycnometer and ground into a paste with a pestle and mortar. The resultant whole ground sample was returned to the pycnometer with water and weighed (pgr). The POR was calculated as follows:
The diameter was measured at the root base with a vernier caliper. Three replicates in each plant were examined.
Relative growth rate and biomass allocation
The relative growth rate (RGR) in plant dry weight was calculated as follows:
where W i and W f are the total dry weights at the beginning and end of the experiment, respectively, and Δt is the experimental period (40 days). The root mass ratio (RMR) was obtained as the root dry weight divided by the total plant dry weight.
Results
Root aerobic respiration
Regardless of plant species, the aerobic respiration rate of roots decreased with a decrease in the dissolved oxygen concentration in the water phase (Fig. 1). The long-term response of root aerobic respiration to hypoxia, however, differed among the species. The root aerobic respiration rate of T. latifolia did not differ between the two growth conditions. In contrast, T. orientalis and T. angustifolia grown under the hypoxic growth condition exhibited significantly higher root aerobic respiration capacities than those grown under the aerobic growth condition (Table 1). The difference was more substantial in T. angustifolia than in T. orientalis.
Root porosity and diameter
The root systems exhibited a compact and dense form under the hypoxic growth condition, irrespective of species. However, the responses of the root anatomy to rhizosphere hypoxia differed among the species (Table 2). T. latifolia and T. orientalis, having high POR, were not affected by the growth conditions, while T. angustifolia increased its POR under the hypoxic growth condition (P<0.05). For root base diameter, a difference was only observed for T. latifolia: the hypoxic growth condition afforded significantly thicker roots (P<0.05).
Growth and biomass allocation
The initial plant dry weights were 5.37±0.81 g, 4.55±0.91 g and 5.49±0.36 g (mean±SD, n=8) for T. latifolia, T. orientalis and T. angustifolia, respectively. During the experimental period, all of the plants of the three Typha species examined survived, but their growth responses to rhizosphere hypoxia were different. RGR values for T. angustifolia and T. orientalis under the hypoxic growth condition were 39% and 59% higher than under the aerobic growth condition, respectively (P<0.05; Table 2). In contrast, the RGR of T. latifolia did not differ significantly between the two growth conditions. T. angustifolia significantly increased its RMR under the hypoxic growth condition (P<0.05), while the RMRs of T. latifolia and T. orientalis did not differ between the two growth conditions. Among the three species, T. latifolia had the highest RMR (P<0.05). Shoot height was not significantly different between the two growth conditions for any of the species (Table 3). The number of leaves per shoot was highest in T. orientalis (P<0.05). T. latifolia and T. angustifolia did not differ in the number of leaves per shoot between the two growth conditions, while in T. orientalis it increased under the hypoxic growth condition (P<0.05).
Discussion
Typha species are plants that inherently grow under anaerobic conditions such as in marshes, swamps and shores of lakes and rivers. The anoxic stress for macrophytes is severe in natural wetlands (DeLaune et al. 1990) compared with the hypoxic growth condition employed in this study (0.02 mmol O2 l−1). Several investigations that used rather mildly hypoxic cultures (Pearson and Havill 1988; Moog and Janiesch 1990; Mark et al. 2001), such as in this study, have suggested that wetland plants exhibit faster growth under the hypoxic growth condition than under the aerobic growth condition because they possess some morphological and physiological mechanisms to overcome the hypoxic stresses.
The three Typha species exhibited different responses of their root aerobic respiration rate to rhizosphere hypoxia. Root aerobic respiration capacities of the deep-water species, T. orientalis and T. angustifolia, increased when they were grown under the hypoxic growth condition, while the shallow-water species T. latifolia was not affected (Fig. 1, Table 1). Moog and Brüggemann (1998) reported for Carex species that the root respiration rates of anaerobically precultured intact plants (roots not detached) were higher than those of aerobically precultured plants. The Carex species studied may have also had an enhanced root aerobic respiration capacity under hypoxia, as was the case for the Typha species in this study, although these authors referred to the possibility that the increase in root respiration rate may be ascribed to an enhanced oxygen supply from shoots derived from altered morphology as a result of hypoxia, such as the development of lacunae (Moog and Brüggemann 1998).
ATP produced in respiratory pathways in roots is partly used for nutrient uptake to support whole plant growth and maintenance. Poorter et al. (1991) investigated 24 herbaceous plants and proved that 50–70% of the energy produced by root respiration was utilized for nutrient uptake. The rates of nutrient uptakes should be closely correlated with photosynthetic capacity and thus the growth rate of whole plants (Kurimoto et al. 2004), since a large amount of nitrogen is needed for the synthesis of photosynthetic enzymes (Poorter et al. 1990). Indeed, high respiratory activities correlated with high growth rates for the 24 herbaceous plants from a wide range of habitats (Poorter et al. 1990), five boreal tree species (Tjoelker et al. 1999), and three wheat and one rice cultivar (Kurimoto et al. 2004). The increased root respiration rates in T. orientalis and T. angustifolia under the hypoxic growth condition also might have promoted nutrient uptake for the development of photosynthetic organs and thus finally resulted in the large biomass yield.
Moog and Janiesch (1990) reported that oxygen deficiency affected production of root biomass in three Carex species from varying hydrological habitats. The extent of oxygen deficiency in their habitats decreased in the following order: Carex extensa, Carex remota L. and Carex pseudocyperus. C. extensa decreased its RMR to reduce respiratory cost versus treated hypoxia. In contrast, C. remota and C. pseudocyperus increased their RMR and formed a compact, dense root network under hypoxia to oxidize the rhizosphere efficiently. This latter finding agrees with this study, as T. angustifolia increased its RMR under the hypoxic growth condition (Table 2), forming a compact, dense root system. An increased RMR results in increased oxygen release from roots to the rhizosphere in as far as the permeability of root surfaces to gases is unchanged. The rhizosphere oxidation will promote efficient conversion from ammonium to nitrate, so that the plants will be able to use sufficient nitrate to support photosynthesis and the growth of the aboveground parts. That T. latifolia had the highest RMR among the three Typha species can be explained partly by the difference in gas permeability of root surfaces.
Hypoxia also alters the root morphology of some wetland plants. Several flooding-tolerant species form aerenchyma at the onset of waterlogging (Smirnoff and Crawford 1983). T. angustifolia experienced an increased POR, and T. latifolia experienced an increased root base diameter in this study (Table 2). Justin and Armstrong (1987) examined the responses to flooding of 91 plant species from wetland, intermediate and non-wetland habitats and proved that unaffected high porosities or raised porosities under flooding are a feature of a majority of wetland and intermediate plants. Increased POR and root diameter would lower the resistance to the diffusion of gases in the root and hence promote aeration in roots and root aerobic respiration. T. orientalis and T. latifolia did not increase their POR in response to hypoxia but exhibited high PORs (ca. 35%) even under the aerated growth condition in this study. This resembles the case of the three juncaceous species and the two cyperaceous species in Justin and Armstrong’s study (1987). Chabbi et al. (2000) reported that the POR of T. domingensis Pers. under a drained growth condition (22%) increased to 28% under a flooded growth condition. A similar increase in POR was observed in T. angustifolia in this study. It is still unclear why different responses of POR and root diameter to hypoxia occur among wetland species such as the three Typha species in this study.
This study has proved that the three Typha species differ in terms of the response of root aerobic respiration rate to hypoxia, and that the difference was closely correlated with their distribution related to water depth. The deep-water species, T. orientalis and T. angustifolia, increased their root aerobic respiration rate by adjusting to hypoxia and grew more rapidly. The shallow-water species, T. latifolia did not show such root respiratory flexibility but maintained almost the same growth rate between the hypoxic and the aerobic growth conditions, at least for the 40 days of the hydroponic culture. Root thickening and other morphological traits not examined in this study might have sustained substantial root respiration and thus growth in T. latifolia.
References
Armstrong J, Armstrong W (1990) Light-enhanced convective throughflow increases oxygenation in rhizomes and rhizosphere of Phragmites australis (Cav.) Trin. ex Steud. New Phytol 114:121–128
Armstrong J, Armstrong W, Beckett PM (1992) Phragmites australis: venturi- and humidity-induced convection enhances rhizome aeration and rhizosphere oxygenation. New Phytol 66:337–347
Armstrong W (1967) The use of polarography in the assay of oxygen diffusing from roots in anaerobic media. Physiol Plant 20:540–553
Armstrong W (1972) A re-examination of the functional significance of aerenchyma. Physiol Plant 27:172–177
Bendix M, Tornbjerg T, Brix H (1994) Internal gas transport in Typha latifolia L. and Typha angustifolia L. I. Humidity-induced pressurization and convective throughflow. Aquat Bot 49:75–89
Brix H, Sorrell BK, Orr PT (1992) Internal pressurization and convective gas flow in some emergent freshwater macrophytes. Limnol Oceanogr 37:1420–1433
Chabbi A, Mckee KL, Mendelssohn IA (2000) Fate of oxygen losses from Typha domingensis (Typhaceae) and Cladium jamaicense (Cyperaceae) and consequences for root metabolism. Am J Bot 87:1081–1090
Cronk JK, Fennessy MS (2001) Wetland plants: biology and ecology. Lewis, Chelsea
Dacey JWH (1980) Internal winds in water lilies: an adaptation for life in anaerobic sediments. Science 210:1017–1019
Dacey JWH (1981) Pressurized ventilation in the yellow waterlily. Ecology 62:1137–1147
DeLaune RD, Pezeshki SR, Pardue. JH (1990) An oxidation-reduction buffer for evaluating the physiological response of plants to oxygen stress. Environ Exp Bot 30:243–247
Grace JB, Wetzel RG (1982) Niche differentiation between two rhizomatous plant species: Typha latifolia and Typha angustifolia. Can J Bot 60:46–57
Grace JB (1988) The effects of nutrient additions on mixtures of Typha latifolia L. and Typha domingensis Pers. along a water-depth gradient. Aquat Bot 31:83–92
Grace JB (1989) Effects of water depth on Typha latifolia and Typha domingensis. Am J Bot 76:762–768
Grosse W (1996) Pressurized ventilation in floating-leaved aquatic macrophytes. Aquat Bot 54:137–150
Jackson MB, Armstrong W (1999) Formation of aerenchyma and the process of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287
Jensen CR, Luxmoore RJ, Van Gundy SD, Stolzy LH (1969) Root air-space measurements by a pycnometer method. Agron J 61:474–475
Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495
Kurimoto K, Day DA, Lambers H, Noguchi K (2004) Effect of respiratory homeostasis on plant growth in cultivars of wheat and rice. Plant Cell Environ 27:853–862
Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer, Berlin Heidelberg New York
Lorenzen J, Larsen LH, Kjær T, Revsbech NP (1998) Biosensor determination of the microscale distribution of nitrate, nitrate assimilation, nitrification, and denitrification in a diatom-inhabited freshwater sediment. Appl Environ Microb 64:3264–3269
Mark RG, John DG, Phillip SC, Timothy DC (2001) Waterlogging tolerance among a diverse range of Trifolium accessions is related to root porosity, lateral root formation and “aerotropic rooting”. Ann Bot 88:579–589
Mendelssohn IA, Postek MT (1982) Elemental analysis of deposits on the roots of Spartina alterniflora Loisel. Am J Bot 69:904–912
Moog PR, Janiesch P (1990) Root growth and morphology of Carex species as influenced by oxygen deficiency. Funct Ecol 4:201–208
Moog PR, Brüggemann W (1998) Flooding tolerance of Carex species. II. Root gas-exchange capacity. Planta 207:199–206
Pearson J, Havill DC (1988) The effect of hypoxia and sulphide on culture-grown wetland and non-wetland plants. I. Growth and nutrient uptake. J Exp Bot 39:363–374
Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol 94:621–627
Poorter H, van der Werf A, Atkin OK, Lambers H (1991) Respiration energy requirements of roots vary with the potential growth rate of a plant species. Physiol Plant 83:469–475
Smirnoff N, Crawford RMM (1983) Variation in the structure and response to flooding of root aerenchyma in some wetland plants. Ann Bot 51:237–249
Sorrell BK, Dromgoole FI (1987) Oxygen transport in the submerged freshwater macrophyte Egeria densa Planch. I. Oxygen production, storage and release. Aquat Bot 28:63–80
Sorrell BK, Armstrong W (1994) On the difficulties of measuring oxygen release by root systems of wetland plants. J Ecol 82:177–183
Sorrell BK, Mendelssohn IA, Mckee KL, Woods RA (2000) Ecophysiology of wetland plant roots: a modeling comparison of aeration in relation to species distribution. Ann Bot 86:675–685
Sorrell BK, Brix H (2003) Effects of water vapour pressure deficit and stomatal conductance on photosynthesis, internal pressurization and convective flow in three emergent wetland plants. Plant Soil 253:71–79
Teal JM, Kanwisher JW (1966) Gas transport in the marsh grass, Spartina alterniflora. J Exp Bot 17:355–361
Tjoelker MG, Oleksyn J, Reich PB (1999) Acclimation of respiration to temperature and CO2 in seedlings of boreal tree species in relation to plant size and relative growth rate. Global Change Biol 49:679–691
Tornbjerg T, Bendix M, Brix H (1994) Internal gas transport in Typha latifolia L. and Typha angustifolia L. II. Convective throughflow pathways and ecological significance. Aquat Bot 49:91–105
Weisner SEB, Granéli W, Ekstam B (1993) Influence of submergence on growth of seedlings of Scirpus lacustris and Phragmites australis. Freshwater Biol 29:371–375
White SD, Ganf GG (1998) The influence of convective flow on rhizome length in Typha domingensis over a water depth gradient. Aquat Bot 62:57–70
Yamasaki S (1984) Role of plant aeration in zonation of Zizania latifolia and Phragmites australis. Aquat Bot 18:287–297
Acknowledgement
The authors thank Dr H. Yura of the Natural History Museum and Institute, Chiba for critical discussion.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Matsui, T., Tsuchiya, T. Root aerobic respiration and growth characteristics of three Typha species in response to hypoxia. Ecol Res 21, 470–475 (2006). https://doi.org/10.1007/s11284-005-0143-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-005-0143-9