Abstract
Plants respond to low nutrient availability by modifying root morphology and root system topology. Root responses to nitrogen (N) and phosphorus (P) limitation may affect plant capacity to withstand water stress. But studies on the effect of nutrient availability on plant ability to uptake and transport water are scarce. In this study, we assess the effect of nitrogen and phosphorus limitation on root morphology and root system topology in Pistacia lentiscus L seedlings, a common Mediterranean shrub, and relate these changes to hydraulic conductivity of the whole root system. Nitrogen and phosphorus deprivation had no effect on root biomass, but root systems were more branched in nutrient limited seedlings. Total root length was higher in seedlings subjected to phosphorus deprivation. Root hydraulic conductance decreased in nutrient-deprived seedlings, and was related to the number of root junctions but not to other architectural traits. Our study shows that changes in nutrient availability affect seedling water use by modifying root architecture. Changes in nutrient availability should be taken into account when evaluating seedling response to drought.
Similar content being viewed by others
References
Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26:1053–1066
Berntson GM (1994) Modelling root architecture: are there tradeoffs between efficiency and potential of resource acquisition? New Phytol 127:483–493
Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants: an economic analogy. Annu Rev Ecol Syst 16:363–392
Bucio JL, Abreu EH, Calderón LS, Jacobo MF, Simpson J, Estrella LH (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256
Caravaca F, Barea JM, Roldán A (2002) Synergistic influence of an arbuscular mycorrhizal fungus and organic amendment on Pistacia lentiscus L. seedlings afforested in a degraded semiarid soil. Soil Biol Biochem 34:1139–1145
Castro-Díez P, Puyravaud JP, Cornelissen JHC, Villar-Salvador P (1998) Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types. Oecologia 116:57–66
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2002) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366
Chirino E, Vilagrosa A, Hernández E, Matos A, Vallejo VR (2008) Effects of a deep container on morpho-functional characteristics and root colonization in Quercus suber L. seedlings for a reforestation in Mediterranean climate. For Ecol Manage 256:779–785
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 51:61–70
Clearwater MJ and Meinzer FC (2001) Relationship between hydraulic architecture and leaf photosynthetic capacity in nitrogen-fertilized Eucalyptus grandis trees. Tree Physiol 21:683–690
Cruiziat P, Cochard H, Améglio T (2002) Hydraulic architecture of trees. Main concepts and results. Ann For Sci 59:723–752
Doussan C, Pagès L, Vercambre G (1998) Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption–distribution of axial and radial conductances in maize. Ann Bot 81:225–232
Eissenstat DM (1997) Trade-offs in root form and function. In: Jackson LE (ed) Ecology and Agriculture. Academic Press, San Diego, pp 173–196
Eissenstat DM, Wells CE, Yanai RD, Withbeck JL (2000) Building roots in changing environment: implications for root longevity. New Phytol 147:33–42
Field CB, Chapin FS III, Matson PA, Mooney HA (1992) Responses of terrestrial ecosystems to the changing atmosphere: a resource-based approach. Annu Rev Ecol Syst 23:201–235
Fiscus EL (1975) The interaction between osmotic- and pressure-induced water flow in plant roots. Plant Physiol 55:917–922
Fitter HA (1991) The ecological significance of root system architecture: an economic approach. In: Atkinson D (ed) Plant root growth: an ecological perspective. Blackwell, Oxford, pp 229–243
Fitter AH, Stickland TR (1991) Architectural analysis of plant root systems. II. Influence of nutrient supply on architecture in contrasting plant species. New Phytol 118:383–389
Fitter AH, Stickland TR, Harvey ML, Wilson GW (1991) Architectural analysis of plant root systems. I. Architectural correlates of exploitation efficiency. New Phytol 118:375–382
Fitter AH, Williamson L, Linkohr B, Leyser O (2002) Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc R Soc Lond B 269:2017–2022
Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Funct Plant Biol 32:737–748
Hsiao TC (1973) Plant responses to water stress. Annu Rev Plant Physiol 24:519–570
Hunt R (1978) Plant growth analysis. Studies in biology no. 96. Edward Arnold, London
Jones B, Ljung K (2012) Subterranean space exploration: the development of root system architecture. Curr Opin Plant Biol 15:97–102
Kramer PJ, Bullock HC (1966) Seasonal variations in the proportion of suberized and unsuberized roots of trees in relation to the absorption of water. Am J Bot 53:200–204
Lal R (2009) Soils and sustainable agriculture. A review. Agron Sustain Dev 28:57–64
Linkohr BI, Williamson LC, Fitter AH, Leyser HMC (2002) Nitrate and phosphate availability and distribution have different effects on root system of architecture of Arabidopsis. Plant J 29:751–760
Loepfe L, Martinez-Vilalta J, Pinola J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol 247:788–803
Lynch JP (1995) Root architecture and plant productivity. Plant Physiol 109:7–13
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Lynch JP, Brown KM (2001) Topsoil foraging: an architectural adaptation to low phosphorus availability. Plant Soil 237:225–237
Lynch JP, Deikman J (1998) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes. American Society of Plant Physiologists, Rockville, MD
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56
Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467
Mac Nally R (2000) Multiple regression and inference in ecology and conservation biology: further comments on identifying important predictor variables. Biodivers Conserv 11:1397–1401
MacFall JS, Johnson GA, Kramer PJ (1991) Comparative water uptake by roots of different ages in seedlings of loblolly pine (Pinus taeda L.). New Phytol 119:551–560
Maestre FT, Cortina J, Bautista S (2004) Mechanisms underlying the interaction between Pinus halepensis and the native late-successional shrub Pistacia lentiscus in a semiarid plantation. Ecography 27:776–786
Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77
Martínez-Vilalta J, Prat E, Oliveras I, Pinol J (2002) Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133:19–29
McCrady RL, Comerford NB (1998) Morphological and anatomical relationships of loblolly pine fine roots. Trees 12:431–437
Nardini A, Salleo S, Lo Gullo MA (1998) Root hydraulic conductance of six forests trees: possible adaptive significance of seasonal changes. Plant Biosyst 132:97–104
Nicotra AB, Babicka N, Westoby M (2002) Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130:136–145
North GB, Baker EA (2007) Water uptake by older roots: evidence from desert succulents. HortScience 42:1103–1107
North GB, Nobel PS (2000) Heterogeneity in water availability alters cellular development and hydraulic conductivity along roots of a desert succulent. Ann Bot 85:247–255
North GB, Ewers FW, Nobel PS (1992) Main-root lateral root junctions of two desert succulents: changes in axial and radial components of hydraulic conductivity during drying. Am J Bot 79:1039–1050
Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495
Passioura JB (1988) Water transport in and to roots. Annu Rev Plant Physiol 39:245–265
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299
Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607
Radin JW (1984) Stomatal responses to water stress and to abscisic acid in phosphorus-deficient cotton plants. Plant Physiol 75:372–377
Radin JW, Ackerson RC (1981) Water relations of cotton plants under nitrogen deficiency III. Stomatal conductance, photosynthesis, and abscisic acid accumulation during drought. Plant Physiol 67:115–119
Radin JW, Eidenbock MP (1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus deficient cotton plants. Plant Physiol 75:771–775
Radin JW, Matthews MA (1989) Water transport properties of cortical cells in roots of nitrogen-and phosphorus-deficient cotton seedlings. Plant Physiol 89:264–268
Robinson D (1996) Variation, co-ordination and compensation in root systems in relation to soil variability. Plant Soil 187:57–66
Rowse HR, Goodman D (1981) Axial resistance to water movement in broad bean (Vici faba) roots. J Exp Bot 32:591–598
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–346
Schulte PJ (2006) Water flow through junctions in Douglas-fir roots. Plant Cell Environ 29:70–76
Schulte PJ, Brooks JR (2003) Branch junctions and the flow of water through xylem in Douglas-fir and ponderosa pine stems. J Exp Bot 74:1438–1445
Shane MW, McCully ME, Canny MJ (2000) Architecture of branch-root junctions in maize: structure of the connecting xylem and porosity of pit membranes. Ann Bot 85:613–624
Simunek J, Hopmans JW (2009) Modeling compensated root water and nutrient uptake. 220:505–520
Sorgonà A, Abenavoli MR, Gringeri PG, Lupini A, Cacco G (2007) Root architecture plasticity of citrus rootstocks in response to nitrate availability. J Plant Nutr 30:1921–1932
Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:115–127
Sperry JS, Ikeda T (1997) Xylem cavitation in roots and stems of Douglas fir and white fir. Tree Physiol 17:275–280
Steudle E (2000) Water uptake by plant roots: an integration of views. Plant Soil 226:45–56
Syvertsen JP, Graham JH (1985) Hydraulic conductivity of roots, mineral nutrition, and leaf gas exchange of citrus root stocks. J Am Soc Hortic Sci 110:865–869
Tan ZX, Lal R, Wiebe KD (2005) Global soil nutrient depletion and yield reduction. J Sustain Agric 26:123–146
Taub DR, Goldberg D (1996) Root system topology of plants from habitats differing in soil resource availability. Funct Ecol 10:258–264
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, Oxford
Tjolker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grasslands and savannah species. New Phytol 167:493–508
Tomaselli R (1981) Main physiognomic types and geographic distribution of shrub systems related to Mediterranean climates. In: di Castri F, Goodall DW, Specht R (eds) Ecosystems of the world, Mediterranean-type shrublands, vol 11. Elsevier Science, Amsterdam, pp 95–106
Trubat R, Cortina J, Vilagrosa A (2006) Plant morphology and root hydraulics are altered by nutrient deficiency in Pistacia lentiscus (L.). Trees 20:334–339
Trubat R, Cortina J, Vilagrosa A (2008) Short-term nitrogen deprivation increases field performance in nursery seedlings of Mediterranean woody species. J Arid Environ 72:879–890
Trubat R, Cortina J, Vilagrosa A (2011) Nutrient deprivation improves field performance of woody seedlings in a degraded semi-arid shrubland. Ecol Eng 37:1164–1173
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360
Valdecantos A, Cortina J, Vallejo VR (2006) Nutrient status and field performance of tree seedlings planted in Mediterranean degraded areas. Ann For Sci 63:249–256
Vilagrosa A, Cortina J, Gil E, Bellot J (2003) Suitability of drought-preconditioning techniques in Mediterranean climate. Restor Ecol 11:208–216
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15
Wells CE, Eissenstat DM (2003) Beyond the roots of young seedlings: the influence of age and order on fine root physiology. J Plant Growth Regul 21:324–334
Werner C, Smart JS (1973) Some new methods of topologic classification of channel networks. Geographical Analysis 5:271–295
Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882
Wu C, Wei X, Sun HL, Wang ZQ (2005) Phosphate availability alters lateral root anatomy and root architecture of Fraxinus mandshurica Rupr. seedlings. J Integr Plant Biol 47:292–301
Zhu J, Ingram PA, Benfey PN, Elich T (2011) From lab to field, new approaches to phenotyping root system architecture. Curr Opin Plant Biol 14:310–317
Zimmermann U (1978) Physics of turgor- and osmoregulation. Annu Rev Plant Physiol 29:121–148
Zimmermann MH (1983) Xylem structure and the ascent sap. Springer, Berlin
Acknowledgments
This research was funded by the CEAM Foundation, the Ministry of Science and Innovation (GRACCIE Program Consolider-Ingenio 2010; SURVIVE CGL2011-30531-C02-02), the Ministry of Environment (RECUVES, 077/RN08/04.1), the EU (FUME project, GA no. 243888) and by the Regional Government of Valencia (FEEDBACKS-PROMETEO/2009/006). CEAM Foundation is funded by Generalitat Valenciana and Fundació Bancaixa. We are grateful to Marian Pérez-Devesa, Juan José Torrecillas, and Santi Soliveres for their help in field work. We are also grateful to Germán Lopez, and Felipe Gil and Conselleria de Medi Ambient, Aigua, Territori i Habitatge for the use of Sta. Faç public nursery.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Marilyn Ball.
Rights and permissions
About this article
Cite this article
Trubat, R., Cortina, J. & Vilagrosa, A. Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings. Oecologia 170, 899–908 (2012). https://doi.org/10.1007/s00442-012-2380-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-012-2380-2