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Root respiratory costs of ion uptake, root growth, and root maintenance in wetland plants: efficiency and strategy of O2 use for adaptation to hypoxia

Abstract

Oxygen use in roots is an important aspect of wetland plant ecophysiology, and it depends on the respiratory costs of three major processes: ion uptake, root growth, and root maintenance. However, O2 allocation in wetland plants has received little attention. This study aimed to determine the O2 allocation and specific respiratory cost of each process under hypoxic conditions, to better understand the strategy and efficiency of O2 use in wetland plants. The root respiration rate, nitrogen uptake, and root growth in three Carex species with different growth rates were examined under hypoxic conditions using different N sources, and the respiratory costs of ion uptake, root growth, and root maintenance were statistically estimated. All species exhibited low specific costs and low ratios of O2 allocation for root growth (2.0 ± 0.4 mmol O2 g−1 and 15.2 ± 2.7 %, respectively). The specific cost of ion uptake was 20–30 % lower in fast-growing species than in slow-growing species. As plant growth rate increased, the O2 allocation ratio for ion uptake increased, and that for root maintenance decreased. The cost was higher when NO3 was fed, than when NH4 + was fed, although the pattern of O2 allocation ratios for three processes was similar for NO3 and NH4 +. Our results indicate that wetland plants primarily employ an O2 use strategy of minimising the respiratory costs of root growth, and fast-growing plants specifically use O2 to maximise ion uptake. These findings provide new insights into ecophysiological behaviours of roots in adaptation to hypoxia.

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References

  1. Aerts R, De Caluwe H, Konings H (1992) Seasonal allocation of biomass and nitrogen in four Carex species from mesotrophic and eutrophic fens as affected by nitrogen supply. J Ecol 80:653–664

  2. Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–332

  3. Armstrong W, Drew M (2002) Root growth and metabolism under oxygen deficiency. In: Weisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker Inc, New York, pp 729–761

  4. Armstrong W, Cousins D, Armstrong J, Turner D, Beckett P (2000) Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. Ann Bot 86:687–703

  5. Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiol 99:1294–1301

  6. Bouma TJ (2005) Understanding plant respiration: separating respiratory components versus a process-based approach. In: Lambers H, Ribas-Carbó M (eds) plant respiration. From cell to ecosystem. Springer, Dordrecht, pp 177–194

  7. Bouma TJ, Broekhuysen AGM, Veen BW (1996) Analysis of root respiration of Solanum tuberosum as related to growth, ion uptake and maintenance of biomass. Plant Physiol Biochem 34:795–806

  8. Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

  9. Britto DT, Kronzucker HJ (2006) Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends Plant Sci 11:529–534

  10. Britto DT, Siddiqi MY, Glass AD, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258

  11. Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309

  12. Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytol 179:964–974

  13. Colmer TD, Voesenek L (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681

  14. De Visser R, Spitters CJT, Bouma T (1992) Energy costs of protein turnover: theoretical calculation and experimental estimation from regression of respiration on protein concentration of full-grown leaves. In: Lambers H, Van der Plas LHW (eds) Molecular, biochemical and physiological aspects of plant respiration. SPB Academic Publishing, The Hague, pp 493–508

  15. Dijkstra P, Lambers H (1989) A physiological analysis of genetic variation in relative growth rate within Plantago major L. Funct Ecol 3:577–587

  16. Elzenga JTM, van Veen H (2010) Waterlogging and plant nutrient uptake. In: Mancuso S, Shabala S (eds) Waterlogging signalling and tolerance in plants. Springer, Berlin, pp 23–35

  17. Greenway H, Gibbs J (2003) Review: mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol 30:999–1036

  18. Kreuzwieser J, Fürniss S, Rennenberg H (2002) Impact of waterlogging on the N-metabolism of flood tolerant and non-tolerant tree species. Plant Cell Environ 25:1039–1049

  19. Kronzucker H, Glass A, Siddiqi M, Kirk G (2000) Comparative kinetic analysis of ammonium and nitrate acquisition by tropical lowland rice: implications for rice cultivation and yield potential. New Phytol 145:471–476

  20. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer, New York

  21. Macuff J, Jarvis S, Cockburn J (1994) Acclimation of NO3 fluxes to low root temperature by Brassica napus in relation to NO3 supply. J Exp Bot 45:1045–1056

  22. Nakamura T, Uemura S, Yabe K (2002a) Hydrochemical regime of fen and bog in north Japanese mires as an influence on habitat and above-ground biomass of Carex species. J Ecol 90:1017–1023

  23. Nakamura T, Uemura S, Yabe K (2002b) Variation in nitrogen-use traits within and between five Carex species growing in the lowland mires of northern Japan. Funct Ecol 16:67–72

  24. Nakamura M, Nakamura T, Tsuchiya T (2010) Advantages of NH4 + on growth, nitrogen uptake and root respiration of Phragmites australis. Plant Soil 331:463–470

  25. Nakamura M, Nakamura T, Tsuchiya T, Noguchi K (2013) Functional linkage between N acquisition strategies and aeration capacities of hydrophytes for efficient oxygen consumption in roots. Physiol Plant 147:135–146

  26. 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

  27. Poorter H, Werf A, Atkin OK, Lambers H (1991) Respiratory energy requirements of roots vary with the potential growth rate of a plant species. Physiol Plant 83:469–475

  28. Scheurwater I, Cornelissen C, Dictus F, Welschen R, Lambers H (1998) Why do fast- and slow-growing grass species differ so little in their rate of root respiration, considering the large differences in rate of growth and ion uptake? Plant, Cell Environ 21:995–1005

  29. Scheurwater I et al (1999) Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant Soil 215:123–134

  30. Scheurwater I, Koren M, Lambers H, Atkin OK (2002) The contribution of roots and shoots to whole plant nitrate reduction in fast- and slow-growing grass species. J Exp Bot 53:1635–1642

  31. Smith A, Hylton C, Koch L, Woolhouse H (1986) Alcohol dehydrogenase activity in the roots of marsh plants in naturally waterlogged soils. Planta 168:130–138

  32. Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates Inc., Sunderland

  33. Ter Steege MW, Stulen I, Wiersema PK, Posthumus F, Vaalburg W (1999) Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux. Plant Soil 208:125–134

  34. Trought M, Drew M (1980) The development of waterlogging damage in young wheat plants in anaerobic solution cultures. J Exp Bot 31:1573–1585

  35. Van der Werf A, Kooijman A, Welschen R, Lambers H (1988) Respiratory energy costs for the maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acutiformis. Physiol Plant 72:483–491

  36. Van der Werf A, Poorter H, Lambers H (1994) Respiration as dependent on a species’ inherent growth rate and on the nitrogen supply to the plant. In: Roy J, Gamier E (eds) A whole plant perspective on carbon-nitrogen interactions. SPB Academic Publishing, The Hague, pp 91–110

  37. Veen B (1979) Energy cost of ion transport. Basic Life Sci 14:187–195

  38. Veen B (1981) Relation between root respiration and root activity. Plant Soil 63:73–76

  39. Wang MY, Siddiqi MY, Ruth TJ, Glass AD (1993) Ammonium uptake by rice roots (I. Fluxes and subcellular distribution of 13NH4 +). Plant Physiol 103:1249–1258

  40. Wang K, Bian S, Jiang Y (2009) Anaerobic metabolism in roots of Kentucky bluegrass in response to short-term waterlogging alone and in combination with high temperatures. Plant Soil 314:221–229

  41. White R (1972) Studies on mineral ion absorption by plants I. The absorption and utilization of phosphate by Stylosanthes humilis, Phaseolus atropurpureus and Desmodium intortum. Plant Soil 36:427–447

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Acknowledgments

We thank Mr. Suguru Saitoh, Mr. Yuhto Koizumi, and Mr. Shin Izawa, Faculty of Bioindustry, Tokyo University of Agriculture, Hokkaido, Japan, for their kind assistance with laboratory work. This study was funded by The Japan Society for the Promotion of Science KAKENHI (Grant Number 24770027).

Author contribution statement

TN and MN conceived and designed the study. TN and MN performed the experiments. TN analysed the data and wrote the manuscript.

Author information

Correspondence to Takatoshi Nakamura.

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The authors declare that they have no conflict of interest.

Additional information

Communicated by Russell K. Monson.

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Nakamura, T., Nakamura, M. Root respiratory costs of ion uptake, root growth, and root maintenance in wetland plants: efficiency and strategy of O2 use for adaptation to hypoxia. Oecologia 182, 667–678 (2016). https://doi.org/10.1007/s00442-016-3691-5

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Keywords

  • Root respiration
  • O2 allocation
  • NH4 +
  • NO3
  • Carex