Abstract
Aims
We investigated how rhizosphere factors (total rhizosphere, roots, arbuscular mycorrhizal fungal hyphae [AMF], and soil solution) and water availability affect interactions between neighboring Medicago sativa plants.
Methods
A three-compartment mesocosm was used to test the effects of rhizosphere factors on plant–plant interactions. A relative interaction index (RII) was calculated to indicate whether effects of neighbor plant on target plant were positive or negative (facilitative or competitive). Isotope tracers were used to test whether AMF hyphae mediated competition for nitrogen (N) between target and neighbor plants.
Results
The effects of rhizosphere factors on the interactions between neighboring M. sativa plants depended on water availability. The effects of total rhizosphere shifted RII from negative to positive as water availability increased. Interaction with the roots and rhizosphere soil solution of neighbor plants shifted RII from negative to positive as water availability increased but the opposite was true for AMF hyphae. AMF hyphae helped neighbor plants compete for 15N when water was available but not when water was limiting.
Conclusions
The effect of total rhizosphere on plant–plant interaction of M. sativa shifted from competitive to facilitative as water availability increased. Competition was reduced by neighboring soil solution and roots but was increased by AMF hyphae.
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References
Armas C, Pugnaire FI (2012) Plant neighbour identity matters to belowground interactions under controlled conditions. PLoS One 6:e27791
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686
Ayres RL, Gange AC, Aplin DM (2006) Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size, and size inequality, of Plantago lanceolata L. J Ecol 94:285–294
Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and rhizobium-meliloti strains, and their effects on growth, N2-fixation (15N) and nutrition of Medicago sativa L. New Phytol 117:399–404
Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Cahill JF Jr (1999) Fertilization effects on interactions between above– and belowground competition in an old field. Ecology 80:466–480
Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349
Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848
Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308
Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol Ecol 73:197–214
Dawson TE (1993) Hydraulic lift and water use by plants: Implications for water balance, performance and plant–plant interactions. Oecologia 95:565–574
Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483
Eränen JK, Kozlov MV (2008) Increasing intraspecific facilitation in exposed environments: consistent results from mountain birch populations in two subarctic stress gradients. Oikos 117:1569–1577
Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gomez-Aparicio L, Zamora R, Gomez JM, Hodar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta–analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138
Hacker S, Bertness M (1999) Experimental evidence for factors maintaining plant species diversity in a new England salt marsh. Ecology 80:2064–2073
Hu S, Chapin FS, Firestone MK, Field CB, Chiariello NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:188–191
Janoušková M, Rydlová J, Püschel D, Száková J, Vosátka M (2011) Extraradical mycelium of arbuscular mycorrhizal fungi radiating from large plants depresses the growth of nearby seedlings in a nutrient deficient substrate. Mycorrhiza 21:641–650
Lerat S, Rachel G, Catford JG, Vierheilig H, Piche’ Y, Lepointe L (2002) 14C transfer between the spring ephemeral Erythronium ameicanum and sugar maple saplings via arbuscular mycorrhizal fungi in natural stands. Oecologia 132:181–187
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus–deficient soils. Proc Natl Acad Sci USA 104:11192–11196
Lortie CJ, Brooker RW, Choler P, Kikvidze Z, Michalet R, Pugnaire FI, Callaway RM (2004) Rethinking plant community theory. Oikos 107:433–438
Lynch JM (1990) The rhizosphere. Wiley, New York
Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valiente-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773
Moora M, Zobel M (1996) Effect of arbuscular mycorrhiza on inter– and intraspecific competition of two grassland species. Oecologia 108:79–84
Moora M, Zobel M (1998) Can arbuscular mycorrhiza change the effect of root competition between conspecific plants of different ages? Can J Bot 76:613–619
Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202
Prieto I, Armas C, Pugnaire FI (2012) Water release through plant roots: new insights into its consequences at the plant and ecosystem level. New Phytol 193:830–841
Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49
Sanders IR, Streitwolf-Engel R, van der Heijden MGA, Boller T, Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment. Oecologia 117:496–503
Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739
Scheublin TR, van Logtestijn RSP, van der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638
Seifan M, Tielbörger K, Kadmon R (2010) Direct and indirect interactions among plants explain counterintuitive positive drought effects on an eastern Mediterranean shrub species. Oikos 119:1601–1609
Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Sandiego
Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbiosis. New Phytol 182:347–358
Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306
Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton
Urcelay C, Diaz S (2003) The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecol Lett 6:388–391
van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Wolfe BE, Weishampel PA, Klironomos JN (2006) Arbuscular mycorrhizal fungi and water table affect wetland plant community composition. J Ecol 94:905–914
Xiao S, Michalet R, Wang G, Chen SY (2009) The interplay between species’ positive and negative interactions shapes the community biomass-species richness relationship. Oikos 118:1343–1348
Yu ZX, Zhang Q, Yang HS, Weiner J, Tang JJ, Chen X (2012) The effects of salt stress and arbuscular mycorrhiza on plant neighbour effects and self-thinning. Basic Appl Ecol 13:673–680
Zhang Q (2011) Plant-plant interactions and arbucular mycorrhizae. PhD thesis
Zhang SS, Jin YL, Tang JJ, Chen X (2009) The invasive plant Solidago canadensis L. suppresses local soil pathogens through allelopathy. Appl Soil Ecol 41:215–222
Zhang Q, Yang RY, Tang JJ, Yang HS, Hu SJ, Chen X (2010) Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PLoS One 5:e12380
Zhang Q, Tang JJ, Chen X (2011a) Plant mortality varies with arbuscular mycorrhizal fungal species identities in a self-thinning population. Biol Lett 7:472–474
Zhang Q, Xu LM, Tang JJ, Bai MG, Chen X (2011b) Arbuscular mycorrhizal mediation of biomass–density relationship of Medicago sativa L. under two water conditions in a field experiment. Mycorrhiza 21:269–277
Acknowledgments
This work was supported by the National Natural Science Foundation of China (NSFC, No. 31070389, 30870405) and the Key Laboratory of Ministry of Agriculture of the People’s Republic of China (No. KYJD09021).
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Responsible Editor: N. Jim Barrow.
Haishui Yang, Zhenxing Yu and Qian Zhang contributed equally to this paper.
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Yang, H., Yu, Z., Zhang, Q. et al. Plant neighbor effects mediated by rhizosphere factors along a simulated aridity gradient. Plant Soil 369, 165–176 (2013). https://doi.org/10.1007/s11104-012-1565-0
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DOI: https://doi.org/10.1007/s11104-012-1565-0