Abstract
Interactions between annual grass and perennial legume species when they are grown together under drought and limited phosphorus (P) availability are likely to be very important for pasture productivity, but are not well understood. Therefore, the objective of this study was to compare the interactions of drought and species combination on growth, nutrition, hydraulic lift and photosynthesis of the Australian native legume Cullen australasicum and the exotic legume Medicago sativa when grown with the exotic annual ryegrass (Lolium rigidum) with poorly soluble FePO4 as the source of P. Plants were grown for 22 weeks in monoculture and in legume-grass mixtures in 1-m tall pots filled with river sand. Two moisture treatments were applied, drought (top 70 cm of soil allowed to dry after 16 weeks of establishment) and control (field capacity). In monoculture, shoot dry weight (DW) pot-1 of L. rigidum was higher than that of C. australasicum and M. sativa. In the mixtures, compared with the monocultures, an increase in shoot DW pot-1 for L. rigidum and a decrease for both C. australasicum and M. sativa resulted in a relative yield total >1. Citrate was the main carboxylate in the rhizosphere of all species, except for the drought-treated L. rigidum in monoculture and mixtures, for which malate was the main constituent. Both C. australasicum and M. sativa had higher concentrations of Ca, Mg, S, Cu, Zn, Mn and Mo in their leaves than did L. rigidum. Hydraulic lift was not detected in M. sativa and C. australasicum; likely reasons are discussed. Photosynthetic rate was similar for all species, but L. rigidum had tighter stomatal control. C. australasicum survived longer under drought than did M. sativa. In conclusion, L. rigidum out-competed the legumes. The legumes provided benefits to the growth of L. rigidum through solubilising P, but not through hydraulic lift. In addition, L. rigidum conserved moisture through tight stomatal control and produced an extensive root system to take up water and nutrients efficiently.
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References
Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007
Bennett RG, Ryan MH, Colmer TD, Real D (2011) Prioritisation of novel pasture species for use in water-limited agriculture: a case study of Cullen in the Western Australian wheatbelt. Genet Resour Crop Evol 58:83–100
Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Bolan NS, Robson AD, Barrow NJ (1987) Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant Soil 99:401–410
Bolland MDA, Gilkes RJ (1998) The relative effectiveness of superphosphate and rock phosphate for soils where vertical and lateral leaching of phosphate occurs. Nutr Cycl Agroecosys 51:139–153
Brady NC, Weil RR (1999) The nature and property of soils. Prentice Hall, Upper Saddle River
Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161
Canals RM, Emeterio LS, Peralta J (2005) Autotoxicity in Lolium rigidum: analyzing the role of chemically mediated interactions in annual plant populations. J Theor Biol 235:402–407
Claassen N, Barber SA (1976) Simulation model for nutrient uptake from soil by a growing plant root system. Agron J 68:961–964
Cocks PS (2001) Ecology of herbaceous perennial legumes: a review of characteristics that may provide management options for the control of salinity and waterlogging in dryland cropping systems. Aust J Agr Res 52:137–151
Corak SJ, Blevins DG, Pallardy SG (1987) Water transfer in an alfalfa/maize association: survival of maize during drought. Plant Physiol 84:582–586
Dear BS, Li GD, Hayes RC, Hughes SJ, Charman N, Ballard RA (2007) Cullen australasicum (syn. Psoralea australasica): a review and some preliminary studies related to its potential as a low rainfall perennial pasture legume. Rangeland J 29:121–132
Elrashidi MA, Larsen S (1978) The effect of phosphate withdrawal by plant and by an anion-exchange resin on the phosphate potential of a soil. Plant Soil 49:323–331
Emeterio LS, Arroyo A, Canals RM (2004) Allelopathic potential of Lolium rigidum Gaud. on the early growth of three associated pasture species. Grass Forage Sci 59:107–112
Espeleta JF, West JB, Donovan LA (2004) Species-specific patterns of hydraulic lift in co-occurring adult trees and grasses in a sandhill community. Oecologia 138:341–349
Gerke J, Beißner L, Römer W (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. J Plant Nutr Soil Sc 163:207–212
Ghannoum O, Conroy JP (2007) Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses. Funct Plant Biol 34:72–81
Gherardi MJ, Rengel Z (2004) The effect of manganese supply on exudation of carboxylates by roots of lucerne (Medicago sativa). Plant Soil 260:271–282
Griffiths FP (1949) Production and utilization of alfalfa. Econ Bot 3:170–183
Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35:241–289
Hatton TJ, Nulsen RA (1999) Towards achieving functional ecosystem mimicry with respect to water cycling in southern Australian agriculture. Agroforest Syst 45:203–214
Hayes RC, Dear BS, Orchard BA, Peoples MB, Eberbach PL (2008) Response of subterranean clover, balansa clover, and gland clover to lime when grown in mixtures on an acid soil. Aust J Agr Res 59:824–835
Henkin Z, Seligman NG, Kafkafi U, Noy-Meir I (1998) ‘Effective growing days’: a simple predictive model of the response of herbaceous plant growth in a Mediterranean ecosystem to variation in rainfall and phosphorus availability. J Ecol 86:137–148
Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286:7–19
Jacob J, Lawlor DW (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42:1003–1011
Jolliffe PA (2000) The replacement series. J Ecol 88:371–385
Jones DL, Darrah PR (1994) Role of root derived organic-acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713
Li L, Li S, Sun J, Zhou L, Bao X, Zhang H, Zhang F (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci 104:11192–11196
Li GD, Lodge GM, Moore GA, Craig AD, Dear BS, Boschma SP, Albertsen TO, Miller SM, Harden S, Hayes RC, Hughes SJ, Snowball R, Smith AB, Cullis BC (2008) Evaluation of perennial pasture legumes and herbs to identify species with high herbage production and persistence in mixed farming zones in southern Australia. Aust J Exp Agr 48:449–466
Lindsay WL (1979) Chemical equilibria in soils. Wiley, New York
Lipton DS, Blanchard RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol 85:315–317
Liste HH, White J (2008) Plant hydraulic lift of soil water – implications for crop production and land restoration. Plant Soil 313:1–17
Lucero DW, Grieu P, Guckert A (1999) Effects of water deficit and plant interaction on morphological growth parameters and yield of white clover (Trifolium repens L.) and ryegrass (Lolium perenne L.) mixtures. Eur J Agron 11:167–177
Lucero DW, Grieu P, Guckert A (2002) Water deficit and plant competition effects on C-14 assimilate partitioning in the plant-soil system of white clover (Trifolium repens L.) and rye-grass (Lolium perenne L.). Soil Biol Biochem 34:1–11
Masaoka Y, Kojima M, Sugihara S, Yoshihara T, Koshino M, Ichihara A (1993) Dissolution of ferric phosphate by alfalfa (Medicago sativa L.) root exudates. Plant Soil 155(156):75–78
Mpelasoka F, Hennessy K, Jones R, Bates B (2008) Comparison of suitable drought indices for climate change impacts assessment over Australia towards resource management. Int J Climatol 28:1283–1292
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL (ed) Methods of soil analysis part 3—chemical methods. Soil Science Society of America, Madison, pp 961–1010
Neumann G, Martinoia E (2002) Cluster roots: an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167
Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130
Pang J, Tibbett M, Denton MD, Lambers H, Siddique KHM, Bolland MDA, Revell CK, Ryan MH (2010) Variation in seedling growth of 11 perennial legumes in response to phosphorus supply. Plant Soil 328:133–143
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288:127–139
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Phys 50:665–693
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49
Raynaud X, Jaillard B, Leadley PW (2008) Plants may alter competition by modifying nutrient bioavailability in rhizosphere: a modeling approach. Am Nat 171:44–58
Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant Cell Environ 23:397–405
Robertson MJ, Carberry PS, Huth NI, Turpin JE, Probert ME, Poulton PL, Bell M, Wright GC, Yeates SJ, Brinsmead RB (2002) Simulation of growth and development of diverse legume species in APSIM. Aust J Agric Res 53:429–446
Robinson K, Bell LW, Bennett RG, Henry DA, Tibbett M, Ryan MH (2007) Perennial legumes native to Australia- a preliminary investigation of nutritive value and response to cutting. Aust J Exp Agr 47:170–176
Rosas A, Rengel Z, Mora ML (2007) Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover. J Plant Nutr 30:253–270
Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Phys 52:527–560
Sanderson MA, Skinner RH, Barker DJ, Edwards GR, Tracy BF, Wedin DA (2004) Plant species diversity and management of temperate forage and grazing land ecosystems. Crop Sci 44:1132–1144
Sandnes A, Eldhuset TD, Wollebaek G (2005) Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biol Biochem 37:259–269
Sardans J, Peñuelas J (2007) Drought changes phosphorus and potassium accumulation patterns in an evergreen Mediterranean forest. Funct Ecol 21:191–201
SAS (2003) SAS/STAT user’s guide, Version 9.1. SAS, Cary
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453
Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–494
Sekiya N, Yano K (2002) Water acquisition from rainfall and groundwater by legume crops developing deep rooting systems determined with stable hydrogen isotope compositions of xylem waters. Field Crop Res 78:133–139
Silberbush M, Barber S (1983) Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant Soil 74:93–100
Skinner RH, Gustine DL, Sanderson MA (2004) Growth, water relations, and nutritive value of pasture species mixtures under moisture stress. Crop Sci 44:1361–1369
Small E (2009) Distribution of perennial Medicago with particular reference to agronomic potential for semiarid Mediterranean climate. In: Bennett SJ (ed) New perennial legumes. University of Western Australia press, Perth, pp 57–80
Smithson PC, Sanchez PA (2001) Plant nutritional problems in marginal soils of developing countries. In: Ae N, Arihara J, Okada K, Srinivasan A (eds) Plant Nutrient Acquisition, New Perspectives. Springer, Tokyo, pp 32–68
Suriyagoda LDB, Ryan MH, Renton M, Lambers H (2010a) Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments. Ann Bot 105:755–767
Suriyagoda LDB, Lambers H, Ryan MH, Renton M (2010b) From controlled environments to field simulations: developing a growth model for the novel perennial pasture legume Cullen australasicum. Agr Forest Meteorol 150:1373–1382
Vance CP, Uhde-Stone C, Dl A (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non renewable resource. New Phytol 157:423–447
Vetterlein D, Marschner H (1993) Use of a microtensiometer technique to study hydraulic lift in a sandy soil planted with pearl millet (Pennisetum americanum (L.) Leeke). Plant Soil 149:275–282
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51
Wan C, Xu W, Sosebee RE, Machado S, Archer T (2000) Hydraulic lift in drought-tolerant and -susceptible maize hybrids. Plant Soil 219:117–126
West JB, Espeleta JF, Donovan LA (2003) Root longevity and phenology differences between two-co-occurring savanna bunchgrasses with different leaf habits. Funct Ecol 17:20–28
Worster CA, Mundt CC (2007) The effect of diversity and spatial arrangement on biomass of agricultural cultivars and native plant species. Basic Appl Ecol 8:521–532
Wouterlood M, Lambers H, Veneklaas EJ (2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Funct Plant Biol 32:153–159
Yoder CK, Nowak RS (1999) Hydraulic lift among native plant species in the Mojave desert. Plant Soil 215:93–102
Young IM (1995) Variation in moisture contents between bulk soil and the rhizosheath of Triticum aestivum L. cv. Wembley. New Phytol 130:135–139
Zhang Z, Rengel Z, Meney K (2007) Growth and resource allocation of Canna indica and Schoenoplectus validus as affected by interspecific competition and nutrient availability. Hydrobiologia 589:235–248
Acknowledgements
We thank two anonymous referees for their valuable suggestions, which greatly improved the manuscript. This study was supported by the School of Plant Biology, and the Future Farm Industries Cooperative Research Centre, The University of Western Australia. LDB Suriyagoda also appreciates the SIRF/UIS Scholarship awarded by the University of Western Australia and further scholarship support from the late Frank Ford. We thank Greg Cawthray for the HPLC analysis, and Michael Smirk for the ICP analysis.
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Suriyagoda, L.D.B., Ryan, M.H., Renton, M. et al. Above- and below-ground interactions of grass and pasture legume species when grown together under drought and low phosphorus availability. Plant Soil 348, 281–297 (2011). https://doi.org/10.1007/s11104-011-0754-6
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DOI: https://doi.org/10.1007/s11104-011-0754-6