Abstract
Background and aims
Overyielding in intercropping compared to monoculture has been widely reported. One of the mechanisms may be the alteration of the microbial community in intercropping and especially the amelioration of the negative effects of pathogens that can accumulate in monocultures. Here we test whether inoculation with arbuscular mycorrhizal fungi (AMF) and wheat take-all disease influences overyielding and whether changes in the microbial communities generate feedbacks on plant growth.
Methods
In Experiment 1, wheat and faba bean were grown in monoculture or intercropping to form three planting patterns. Plants were inoculated with or without wheat take-all disease (Gaeumannomyces graminis), and one, six, or no AM fungi, to create 6 soil conditioned treatments. Soils from Experiment 1 were used as inocula in Experiment 2 to test the feedback on plant growth from monocultures and the legacy benefits of intercropping.
Results
No significant influence of AMF on plant growth was observed in either experiment. In Experiment 1, AMF had no significant effect in suppressing take-all but take-all tended to decrease AMF colonization. Shoot biomass and competitive ability of wheat was suppressed by take-all in both experiments. Wheat and faba bean showed overyielding in both the take-all and non-take-all treatment in Experiment 1 but only overyielding in the take-all treatment in Experiment 2. Growth of wheat and faba bean were suppressed in conspecific soil, and this negative feedback was observed across all take-all and AMF treatments, and regardless of competition. Biomass of wheat and faba bean was higher in soil from intercropping than in monoculture soil, and this positive legacy benefit of intercropping did not depend on take-all, AMF or plant competition.
Conclusions
We find support for alterations of the soil community causing negative plant soil feedback and positive legacy benefits of intercropping. Our results are consistent with microbial dynamics generating overyielding in intercropping by reducing the negative influence of soil pathogen build-up on conspecific host plants and simultaneously compensatively improving growth of neighbor plants.
Similar content being viewed by others
References
Agegnehu G, Ghizaw A, Sinebo W (2008) Yield potential and land-use efficiency of wheat and faba bean mixed intercropping. Agron Sustain Dev 28:257–263
Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020
Bedoussac L, Journet EP, Hauggaard-Nielsen H, Naudin C, Corre-Hellou G, Jensen E, Prieur L, Justes E (2015) Ecological principles underlying the increase of productivity achieved by cereal-grain legume intercrops in organic farming. A review. Agron Sustain Dev 35:911–935
Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977
Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. P Roy Soc B Biol Sci 269:2595–2601
Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473
Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573
Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283
Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325. doi:10.1146/annurev-ecolsys-112414-054306
Bradley DJ, Gilbert GS, Martiny JBH (2008) Pathogens promote plant diversity through a compensatory response. Ecol Lett 11:461–469
Brinkman EP, van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073
Brooker RW, Bennett AE, Cong WF, Daniell TJ, George TS, Hallett PD, Hawes C, Iannetta PP, Jones HG, Karley AJ, Li L, Mckenzie BM, Pakeman RJ, Paterson E, Schöb C, Shen JB, Squire G, Watson CA, Zhang CC, Zhang FS, Zhang JL, White PJ (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206:107–117
Casper BB, Castelli JP (2007) Evaluating plant-soil feedback together with competition in a serpentine grassland. Ecol Lett 10:394–400
Castelli JP, Casper BB (2003) Intraspecific AM fungal variation contributes to plant-fungal feedback in a serpentine grassland. Ecology 84:323–336
Creissen HE, Jorgensen TH, Brown JK (2015) Impact of disease on diversity and productivity of plant populations. Funct Ecol 30:649–657
Creissen HE, Jorgensen TH, Brown JK (2016) Increased yield stability of field-grown winter barley (Hordeum vulgare L.) varietal mixtures through ecological processes. Crop Prot 85:1–8
Deberdt P, Perrin B, Coranson-Beaudu R, Duyck PF, Wicker E (2012) Effect of Allium fistulosum extract on Ralstonia solanacearum populations and tomato bacterial wilt. Plant Dis 96:687–692
Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Res 30:75–115
Gao X, Wu M, Xu RN, Wang XR, Pan RQ, Kim HJ, Liao H (2014) Root interactions in a maize/soybean intercropping system control soybean soil-borne disease, red crown rot. PLoS One 9:e95031
Gilbert GS (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol 40:13–43
Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Hao ZP, Christie P, Qin L, Wang CX, Li XL (2005) Control of fusarium wilt of cucumber seedlings by inoculation with an arbuscular mycorrhical fungus. J Plant Nutr 28:1961–1974
Hao WY, Ren LX, Ran W, Shen QR (2010) Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.Sp. niveum. Plant Soil 336:485–497
Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257
Hauggaard-Nielsen H, Jensen ES (2005) Facilitative root interactions in intercrops. Plant Soil 274:237–250
He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706
Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O'Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127
Hendriks M, Mommer L, de Caluwe H, Smit-Tiekstra AE, van der Putten WH, de Kroon H (2013) Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding. J Ecol 101:287–297
Hol WHG, de Boer W, ten Hooven F, van der Putten WH (2013) Competition increases sensitivity of wheat (Triticum aestivum) to biotic plant-soil feedback. PLoS One 8:e66085
Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
Kulmatiski A, Beard KH, Heavilin J (2012) Plant-soil feedbacks provide an additional explanation for diversity-productivity relationships. P Roy Soc B Biol Sci 279:3020–3026
Lankau RA (2012) Coevolution between invasive and native plants driven by chemical competition and soil biota. P Natl Acad Sci USA 109:11240–11245
Latz E, Eisenhauer N, Rall BC, Allan E, Roscher C, Scheu S, Jousset A (2012) Plant diversity improves protection against soil-borne pathogens by fostering antagonistic bacterial communities. J Ecol 100:597–604. doi:10.1111/j.1365-2745.2011.01940.x
Li L, Sun JH, Zhang FS, Guo TW, Bao XG, Smith FA, Smith SE (2006) Root distribution and interactions between intercropped species. Oecologia 147:280–290
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. P Natl Acad Sci USA 104:11192–11196
Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69
Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. P Natl Acad Sci USA 113:6496–9501
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
Mangan SA, Herre EA, Bever JD (2010) Specificity between Neotropical tree seedlings and their fungal mutualists leads to plant–soil feedback. Ecology 91:2594–2603
Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41
Monfort E, Lopez-Llorca LV, Jansson HB, Salinas J, Park JO, Sivasithamparam K (2005) Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot. Soil Biol Biochem 37:1229–1235
Muler AL, Oliveira RS, Lambers H, Veneklaas EJ (2014) Does cluster-root activity benefit nutrient uptake and growth of co-existing species? Oecologia 174:23–31
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457
Ren LX, Su SM, Yang XM, Xu YC, Huang QW, Shen QR (2008) Intercropping with aerobic rice suppressed Fusarium wilt in watermelon. Soil Biol Biochem 40:834–844
Ren L, Lou Y, Sakamoto K, Inubushi K, Amemiya Y, Shen Q, Xu G (2010) Effects of arbuscular mycorrhizal colonization on microbial community in rhizosphere soil and Fusarium wilt disease in tomato. Commun Soil Sci Plant Anal 41:1399–1410
Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291
Rottstock T, Joshi J, Kummer V, Fischer M (2014) Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:1907–1917
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
Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA, van Nes EH, Scheffer M (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303
Siasou E, Standing D, Killham K, Johnson D (2009) Mycorrhizal fungi increase biocontrol potential of Pseudomonas fluorescens. Soil Biol Biochem 41:1341–1343
Sillero JC, Villegas-Fernández AM, Thomas J, Rojas-Molina MM, Emeran AA, Fernández-Aparicio M, Rubiales D (2010) Faba bean breeding for disease resistance. Field Crops Res 115:297–307
Song Y, Zhang F, Marschner P, Fan F, Gao H, Bao X, Sun J, Li L (2007) Effect of intercropping on crop yield and chemical and microbiological properties in rhizosphere of wheat (Triticum aestivum L.), maize (Zea mays L.), and faba bean (Vicia faba L.). Bio Fert Soils 43:565–574
Sun YM, Zhang NN, Wang ET, Yuan HL, Yang JS, Chen WX (2009) Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.). FEMS Microbiol Ecol 70:218–226
Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845
van der Putten WH, Kowalchuk GA, Brinkman EP, Doodeman GTA, van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88:978–988
van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276
Wang ZG, Bao XG, Li XF, Jin X, Zhao JH, Sun JH, Christie P, Li L (2015) Intercropping maintains soil fertility in terms of chemical properties and enzyme activities on a timescale of one decade. Plant Soil 391:265–282
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
Zhao J, Zeng ZX, He XY, Chen HS, Wang KL (2015) Effects of monoculture and mixed culture of grass and legume forage species on soil microbial community structure under different levels of nitrogen fertilization. Eur J Soil Biol 68:61–68
Zhu YY, Chen HR, Fan JH, Wang YY, Li Y, Chen JB, Fan JX, Yang SS, Hu LP, Leung H, Mew TW, Teng PS, Wang ZH, Mundt CC (2000) Genetic diversity and disease control in rice. Nature 406:718–722
Zuo YM, Zhang FS, Li XL, Cao YP (2000) Studies on the improvement in iron nutrition of peanut by intercropping with maize on a calcareous soil. Plant Soil 220:13–25
Acknowledgements
This work was funded by the Projects of the International Cooperation and Exchanges Program of NSFC (31210103906), the State Key Basic Research and Development Plan of China (2015CB150405), and the National Natural Science Foundation of China (Grant Nos. 31272251, 31421092). Guangzhou Wang thanks the China Scholarship Council for a Visiting Scholarship. We thank Professor Youshan Wang (Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry Research, Beijing, China) for providing us with the AMF inoculum and Professor Zhensheng Kang (College of Plant Protection, Northwest A & F University, Shaanxi, China) for the take-all.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Gera Hol.
Electronic supplementary material
ESM 1
(DOCX 664 kb)
Rights and permissions
About this article
Cite this article
Wang, G.Z., Li, H.G., Christie, P. et al. Plant-soil feedback contributes to intercropping overyielding by reducing the negative effect of take-all on wheat and compensating the growth of faba bean. Plant Soil 415, 1–12 (2017). https://doi.org/10.1007/s11104-016-3139-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-3139-z