Oecologia

, Volume 143, Issue 2, pp 189–197

Root hydraulic conductivity and whole-plant water balance in tropical saplings following a shade-to-sun transfer

Ecophysiology

Abstract

We hypothesized that pioneer and late successional species show different morphological and physiological responses in water use after gap formation. The magnitude of the responses was compared between two pioneer species (Macaranga gigantea and Trema orientalis) and four late successional species (Shorea sp.), in an experiment in which saplings were transferred from shade to sun. Although transpiration demand increased following the transfer, root hydraulic conductivity (Lpr) decreased. Lpr was sensitive to brief treatments with HgCl2 (a specific inhibitor of aquaporins). This allows Lpr to be divided into two components: cell-to-cell and apoplastic pathways. The Lpr of cell-to-cell pathway decreased in all species following the transfer, relating to aquaporin depression in roots. Following the transfer, leaf osmotic potentials at full hydration decreased and both leaf mass per area [leaf mass/leaf area (LMA)] and fine-root surface area/leaf surface area (root SA/leaf SA) increased in almost all species, allowing saplings to compensate for the decrease in Lpr. Physiologically, pioneer species showed larger decreases in Lpr and more effective osmotic adjustment than late successional species, and morphologically, pioneer species showed larger increases in root SA/leaf SA and LMA. Water balance at the whole-plant level should be regulated by coupled responses between the aboveground and the belowground parts. Interspecific differences in responses after gap formation suggest niche differentiation in water use between pioneer and late successional species in accordance with canopy-gap size.

Keywords

Aquaporins Dry matter allocation Leaf mass per area Leaf osmotic potential Niche differentiation 

References

  1. Barrowclough DE, Peterson CA, Steudle E (2000) Radial hydraulic conductivity along developing onion roots. J Exp Bot 51:547–557Google Scholar
  2. Bazzaz FA, Pickett STA (1980) Physiological ecology of tropical succession: a comparative review. Annu Rev Ecol Syst 11:287–310Google Scholar
  3. Bonnett HT (1968) The root endodermis: fine structure and function. J Cell Biol 37:199–205Google Scholar
  4. Brokaw NVL (1985) Gap-phase regeneration in a tropical forest. Ecology 66:682–687Google Scholar
  5. Carvajal M, Cooke DT, Clarkson DT (1996) Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199:372–381Google Scholar
  6. Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57Google Scholar
  7. Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70Google Scholar
  8. Denslow JS (1980) Gap partitioning among tropical rainforest trees. Biotropica 12:47–55Google Scholar
  9. Grubb PJ (1977) The maintenance of species-richness in plant communities. Bio Rev 52:107–145Google Scholar
  10. Henzler T, Waterhouse RN, Smyth AJ, Carvajal M, Cooke DT, Schäffner AR, Steudle E, Clarkson DT (1999) Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210:50–60Google Scholar
  11. Ishida A, Yamamura Y, Hori Y (1992) Roles of leaf water potential and soil-to-leaf hydraulic conductance in water-use by understorey woody plants. Ecol Res 7:213–223Google Scholar
  12. Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–303Google Scholar
  13. Kamaluddin M, Zwiazek JJ (2001) Metabolic inhibition of root water flow in red-osier dogwood (Cornus stolonifera) seedlings. J Exp Bot 52:739–745Google Scholar
  14. Maggio A, Joly RJ (1995) Effects of mercuric chloride on the hydraulic conductivity of tomato root systems. Plant Physiol 109:331–335Google Scholar
  15. Maherali H, DeLucia EH, Sipe TW (1997) Hydraulic adjustment of maple saplings to canopy gap formation. Oecologia 112:472–480Google Scholar
  16. Martínez-Ballesta MC, Aparicio F, Pallás V, Martínez V, Carvajal M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J Plant Physiol 160:689–697Google Scholar
  17. Martre P, North GB, Nobel PS (2001) Hydraulic conductance and mercury-sensitive water transport for roots of Opuntia acanthocarpa in relation to soil drying and rewetting. Plant Physiol 126:352–362Google Scholar
  18. Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110Google Scholar
  19. Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J 14:3028–3035Google Scholar
  20. Morgan MD (1971) Life history and energy relationships of Hydrophyllum appendiculatum. Ecol Monogr 41:329–349Google Scholar
  21. Naidu SL, DeLucia EH (1997) Growth, allocation and water relations of shade-grown Quercus ruercus rubra L. saplings exposed to a late-season canopy gap. Ann Bot 80:335–344Google Scholar
  22. Niinemets Ü, Sober A, Kull O, Hartung W, Tenhunen JD (1999) Apparent controls on leaf conductance by soil water availability and via light-acclimation of foliage structural and physiological properties in a mixed deciduous, temperature forest. Int J Plant Sci 160:707–721Google Scholar
  23. North GB, Nobel PS (2000) Heterogeneity in water availability alters celluar development and hydraulic conductivity along roots of a desert succulent. Ann Bot 85:247–255Google Scholar
  24. North GB, Martre P, Nobel PS (2004) Aquaporins account for variations in hydraulic conductance for metabolically active root regions of Agave deserti in wet, dry, and rewetted soil. Plant Cell Environ 27:219–228Google Scholar
  25. Olivares E, Medina E (1992) Water and nutrient relations of woody perennials from tropical dry forests. J Veg Sci 3:383–392Google Scholar
  26. Paz H (2003) Root/shoot allocation and root architecture in seedlings: variation among forest sites, microhabitats, and ecological groups. Biotropica 35:318–332Google Scholar
  27. Rieger M, Litvin P (1999) Root system hydraulic conductivity in species with contrasting root anatomy. J Exp Bot 50:201–209Google Scholar
  28. Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280CrossRefGoogle Scholar
  29. Steudle E (1993) Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell, tissue, and organ level. In: Smith JAC, Griffith H (eds) Water deficits: plant responses from cell to community. Bios Scientific Publishers, Oxford, pp 5–36Google Scholar
  30. Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542CrossRefPubMedGoogle Scholar
  31. Steudle E, Frensch J (1996) Water transport in plants: role of the apoplast. Plant Soil 187:67–79Google Scholar
  32. Steudle E, Meshcheryakov AB (1996) Hydraulic and osmotic properties of oak roots. J Exp Bot 47:387–401Google Scholar
  33. Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788CrossRefGoogle Scholar
  34. Strauss-Debenedetti S, Bazzaz FA (1991) Plasticity and acclimation to light in tropical Moraceae of different successional positions. Oecologia 87:377–387Google Scholar
  35. T, Kudoh H, Kachi N (2003) Responses of root length/leaf area ratio and specific root length of an understory herb, Pteridophyllum racemosum, to increases in irradiance. Plant Soil 255:227–237Google Scholar
  36. Tazawa M, Ohkuma E, Shibasaka M, Nakashima S (1997) Mercurial-sensitive water transport in barley roots. J Plant Res 110:435–442Google Scholar
  37. Turner NC, Jones MM (1980) Turgor maintenance by osmotic adjustment: a review and evaluation. In: Turner NC, Kramer PJ (eds) Adaptation of plants to water and high temperature stress. Wiley, Hoboken, pp 87–103Google Scholar
  38. Tyree MT, Velez V, Dalling JW (1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114:293–298Google Scholar
  39. Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936Google Scholar
  40. Wan X, Zwiazek JJ (1999) Mercuric chloride effects on root water transport in aspen seedlings. Plant Physiol 121:939–946Google Scholar
  41. Weatherley PE (1982) Water uptake and flow into roots. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology, vol 12B. Springer, Berlin Heidelberg New York, pp 79–109Google Scholar
  42. Whitmore TC (1998) An introduction to tropical rain forests, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  43. Yamashita N, Ishida A, Kushima H, Tanaka N (2000) Acclimation to sudden increase in light favoring an invasive over native trees in subtropical islands, Japan. Oecologia 125:412–419Google Scholar
  44. Zhang W-H, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120:849–857Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Michiru Shimizu
    • 1
  • Atsushi Ishida
    • 2
  • Taizo Hogetsu
    • 1
  1. 1.Graduate school of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  2. 2.Department of Plant EcologyForestry and Forest Products Research Institute (FFPRI)TsukubaJapan

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