Abstract
Aim
Cereal/legume intercropping often increases yield, partly because of increased nitrogen (N) and phosphorus (P) acquisition. The aim of this paper was to investigate the role of arbuscular mycorrhizal (AM) fungal common mycorrhizal networks (CMNs) in overyielding by the millet (Setaria italica L.) and chickpea (Cicer arietinum L.) mixture and to find out if the effect of a CMN depends on which of the two species was first colonized by AM fungi (AMF).
Methods
Microcosms with two compartments were used, separated by a 30-μm nylon mesh. Both compartments contained either chickpea or millet, in monoculture or mixed. One or none of the two compartments was inoculated with the AMF species Funneliformis mosseae. The plant in the inoculated compartment was referred to as the donor, and the plant in the neighboring, non-inoculated compartment as the receiver.
Results
Inoculation in one compartment resulted in mycorrhiza formation in the other compartment, providing evidence for the formation of CMNs. Inoculation of chickpea in the mixture increased N and P acquisition and biomass of both chickpea (donor) and millet (receiver) leading to overyielding of the mixture, whereas inoculation of millet increased biomass of chickpea (receiver) only, but did not increase N or P acquisition by any of the two species, and there was no overyielding. Chickpea as donor had higher numbers of phosphate-solubilizing bacteria in its rhizosphere compared to chickpea as receiver. The shoot N:P ratio of chickpea as donor was lower than as receiver.
Conclusion
Our study demonstrated asymmetry in nutrient gains by a mixture of a cereal and a legume, dependent on which plant species was the donor or receiver. This suggests that initiating mycorrhizal networks by legumes in intercropping could be an important factor contributing to the magnitude of the intercropping effect.
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References
Betencourt E, Duputel M, Colomb B, Desclaux D, Hinsinger P (2012) Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil. Soil Biol Biochem 46:181–190. https://doi.org/10.1016/j.soilbio.2011.11.015
Brooker RW, Bennett AE, Cong W-F, Daniell TJ, George TS, Hallett PD, Hawes C, Iannetta PPM, Jones HG, Karley AJ, Li L, McKenzie BM, Pakeman RJ, Paterson E, Schöb C, Shen J, Squire G, Watson CA, Zhang C et al (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206(1):106–117. https://doi.org/10.1111/nph.13132
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157. https://doi.org/10.3389/fpls.2019.00157
Cheng X, Baumgartner K (2004) Arbuscular mycorrhizal fungi-mediated nitrogen transfer from vineyard cover crops to grapevines. Biol Fert Soils 40(6):406–412. https://doi.org/10.1007/s00374-004-0797-4
Daniell TJ, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36(2–3):203–209. https://doi.org/10.1016/s0168-6496(01)00134-9
Ding X, Sui X, Wang F, Gao J, He X, Zhang F, Yang J, Feng G (2012) Synergistic interactions between Glomus mosseae and Bradyrhizobium japonicum in enhancing proton release from nodules and hyphae. Mycorrhiza 22(1):51–58. https://doi.org/10.1007/s00572-011-0381-3
Duchene O, Vian JF, Celette F (2017) Intercropping with legume for agroecological cropping systems: complementarity and facilitation processes and the importance of soil microorganisms. A review Agr Ecosyst Environ 240:148–161. https://doi.org/10.1016/j.agee.2017.02.019
Fan FL, Zhang FS, Song YN, Sun JH, Bao XG, Guo TW, Li L (2006) Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283(1–2):275–286. https://doi.org/10.1007/s11104-006-0019-y
Faucon MP, Houben D, Reynoird JP, Mercadal-Dulaurent AM, Armand R, Lambers H (2015) Advances and Perspectives to Improve the Phosphorus Availability in Cropping Systems for Agroecological Phosphorus Management. In: Sparks DL (ed) Advances in Agronomy, vol 134. pp 51–79. doi:https://doi.org/10.1016/bs.agron.2015.06.003
Frey B, Schüepp H (1993) A role of vesicular-arbuscular (VA) mycorrhizal fungi in facilitating interplant nitrogen transfer. Soil Biol Biochem 25(6):651–658. https://doi.org/10.1016/0038-0717(93)90104-J
Gahan J, Schmalenberger A (2015) Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization. Appl Soil Ecol 89:113–121. https://doi.org/10.1016/j.apsoil.2014.12.008
Güsewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164(2):243–266. https://doi.org/10.1111/j.1469-8137.2004.01192.x
He X-H, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22(6):531–567. https://doi.org/10.1080/713608315
Hu JL, Li MH, Liu HM, Zhao Q, Lin XG (2019) Intercropping with sweet corn (Zea mays L. var. rugosa Bonaf.) expands P acquisition channels of chili pepper (Capsicum annuum L.) via arbuscular mycorrhizal hyphal networks. J Soils Sediments 19(4):1632–1639. https://doi.org/10.1007/s11368-018-2198-6
Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates - Solubilization mechanisms. Soil Biol Biochem 27(3):257–263. https://doi.org/10.1016/0038-0717(94)00190-C
Jia Y, Gray VM, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann Bot-London 94(2):251–258. https://doi.org/10.1093/aob/mch135
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Buecking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880–882. https://doi.org/10.1126/science.1208473
Legay N, Grassein F, Binet MN, Arnoldi C, Personeni E, Perigon S, Poly F, Pommier T, Puissant J, Clement JC, Lavorel S, Mouhamadou B (2016) Plant species identities and fertilization influence on arbuscular mycorrhizal fungal colonisation and soil bacterial activities. Appl Soil Ecol 98:132–139. https://doi.org/10.1016/j.apsoil.2015.10.006
Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016a) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. P Natl Acad Sci USA 113(23):6496–6501. https://doi.org/10.1073/pnas.1523580113
Li C (2020) Phosphorus acquisition and yield gain in intercropping: empirical studies and meta-analysis. Wageningen University, Wageningen
Li C, Hoffland E, Kuyper TW, Yu Y, Li H, Zhang C, Zhang F, van der Werf W (2020a) Yield gain, complementarity and competitive dominance in intercropping in China: A meta-analysis of drivers of yield gain using additive partitioning. Eur J Agron 113. doi:https://doi.org/10.1016/j.eja.2019.125987
Li C, Hoffland E, Kuyper TW, Yu Y, Zhang C, Li H, Zhang F, van der Werf W (2020b) Syndromes of production in intercropping impact yield gains. Nat Plants 6:653–660. https://doi.org/10.1038/s41477-020-0680-9
Li C, Hoffland E, van der Werf W, Zhang J, Li H, Sun J, Zhang F, Kuyper TW (2021a) Complementarity and facilitation with respect to P acquisition do not drive overyielding by intercropping. Field Crops Res 265:108127. https://doi.org/10.1016/j.fcr.2021.108127
Li C, Kuyper TW, van der Werf W, Zhang J, Li H, Zhang F, Hoffland E (2019) Testing for complementarity in phosphorus resource use by mixtures of crop species. Plant Soil 439(1–2):163–177. https://doi.org/10.1007/s11104-018-3732-4
Li C, Kuyper TW, van der Werf W, Zhang J, Li H, Zhang F, Hoffland E (2021b) A conceptual framework and an empirical test of complementarity and facilitation with respect to P uptake by species mixtures. Pedosphere In press
Li CJ, Dong Y, Li HG, Shen JB, Zhang FS (2016b) Shift from complementarity to facilitation on P uptake by intercropped wheat neighboring with faba bean when available soil P is depleted. Sci Rep 6. doi: Artn1866310.1038/Srep18663
Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203(1):63–69. https://doi.org/10.1111/nph.12778
Li M, Hu J, Lin X (2021c) The roles and performance of arbuscular mycorrhizal fungi in intercropping systems. Soil Ecol Lett. https://doi.org/10.1007/s42832-021-0107-1
Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot-London 94(2):297–303. https://doi.org/10.1093/Aob/Mch140
Li YF, Ran W, Zhang RP, Sun SB, Xu GH (2009) Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mung bean intercropping system. Plant Soil 315(1–2):285–296. https://doi.org/10.1007/s11104-008-9751-9
Liu YC, Qin XM, Xiao JX, Tang L, Wei CZ, Wei JJ, Zheng Y (2017) Intercropping influences component and content change of flavonoids in root exudates and nodulation of Faba bean. J Plant Interact 12(1):187–192. https://doi.org/10.1080/17429145.2017.1308569
Lopez-Bellido FJ, Lopez-Bellido RJ, Redondo R, Lopez-Bellido L (2010) B value and isotopic fractionation in N-2 fixation by chickpea (Cicer arietinum L.) and faba bean (Vicia faba L.). Plant Soil 337(1–2):425–434. https://doi.org/10.1007/s11104-010-0538-4
Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6(May):1–10. https://doi.org/10.3389/fpls.2015.00339
Moora M, Zobel M (1996) Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia 108(1):79–84. https://doi.org/10.1007/BF00333217
Neumann G (2006) Quantitative determination of acid phosphatase activity in the rhizosphere and on the root surface. Handbook of Methods used in Rhizosphere Research:pp.536
Phillips J, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160. https://doi.org/10.1016/S0007-1536(70)80110-3
Pinheiro JC, Bates DJ, DebRoy S, Sakar D, R Core Team (2020) _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 31–151 <URL: https://CRAN.R-project.org/package=nlme>
Qiao X, Bei S, Li C, Dong Y, Li H, Christie P, Zhang F, Zhang J (2015) Enhancement of faba bean competitive ability by arbuscular mycorrhizal fungi is highly correlated with dynamic nutrient acquisition by competing wheat. Sci Rep 5. doi:https://doi.org/10.1038/srep08122
Qiao X, Bei SK, Li HG, Christie P, Zhang FS, Zhang JL (2016) Arbuscular mycorrhizal fungi contribute to overyielding by enhancing crop biomass while suppressing weed biomass in intercropping systems. Plant Soil 406(1–2):173–185. https://doi.org/10.1007/s11104-016-2863-8
Ryan MH, Tibbett M, Edmonds-Tibbett T, Suriyagoda LDB, Lambers H, Cawthray GR, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35(12):2170–2180. https://doi.org/10.1111/j.1365-3040.2012.02547.x
Shearer G, Kohl D (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13(6):699–756. https://doi.org/10.1071/PP9860699
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Elsevier Academic Press Inc, San Diego
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61(2):295–304. https://doi.org/10.1111/j.1574-6941.2007.00337.x
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(1):1–45. https://doi.org/10.1023/A:1015798428743
Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92(6):1303–1313. https://doi.org/10.1890/10-1915.1
Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159(2):789–797. https://doi.org/10.1104/pp.112.195727
Wang G, Ye C, Zhang J, Koziol L, Bever JD, Li X (2019) Asymmetric facilitation induced by inoculation with arbuscular mycorrhizal fungi leads to overyielding in maize/faba bean intercropping. J Plant Interact 14(1):10–20. https://doi.org/10.1080/17429145.2018.1550218
Wang X-X, Hoffland E, Feng G, Kuyper TW (2020) Arbuscular mycorrhizal symbiosis increases phosphorus uptake and productivity of mixtures of maize varieties compared to monocultures. J Appl Ecol 57(11):2203–2211. https://doi.org/10.1111/1365-2664.13739
Wang X, Deng X, Pu T, Song C, Yong T, Yang F, Sun X, Liu W, Yan Y, Du J (2017) Contribution of interspecific interactions and phosphorus application to increasing soil phosphorus availability in relay intercropping systems. Field Crops Res 204:12–22. https://doi.org/10.1016/j.fcr.2016.12.020
Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223:882–895. https://doi.org/10.1111/nph.15833
Weremijewicz J, Janos DP (2013) Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol 198(1):203–213. https://doi.org/10.1111/nph.12125
Weremijewicz J, Sternberg LSLOR, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212(2):461–471. https://doi.org/10.1111/nph.14041
Weremijewicz J, Sternberg LSLOR, Janos DP (2018) Arbuscular common mycorrhizal networks mediate intra- and interspecific interactions of two prairie grasses. Mycorrhiza 28(1):71–83. https://doi.org/10.1007/s00572-017-0801-0
Werner GDA, Kiers ET (2015a) Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol 205(4):1515–1524. https://doi.org/10.1111/nph.13092
Werner GDA, Kiers ET (2015b) Partner selection in the mycorrhizal mutualism. New Phytol 205(4):1437–1442. https://doi.org/10.1111/nph.13113
Willey RW (1990) Resource use in intercropping systems. Agr Water Manage 17(1–3):215–231. https://doi.org/10.1016/0378-3774(90)90069-B
Workman RE, Cruzan MB (2016) Common mycelial networks impact competition in an invasive grass. Amer J Bot 103(6):1041–1049. https://doi.org/10.3732/ajb.1600142
Xing F, Gao M, Zhuo Y, Hu Z, Li X (2016) Screening and identification of phosphate solubilizing bacteria in maize rhizosphere and their characteristics of phosphate solubilizing. Chin Agric Sci Bulletin (in Chinese) 32:119–124
Xue Y, Xia H, Christie P, Zhang Z, Li L, Tang C (2016) Crop acquisition of phosphorus, iron and zinc from soil in cereal/legume intercropping systems: a critical review. Ann Bot-London 117(3):363–377. https://doi.org/10.1093/aob/mcv182
Zhang C, Dong Y, Tang L, Zheng Y, Makowski D, Yu Y, Zhang F, van der Werf W (2019) Intercropping cereals with faba bean reduces plant disease incidence regardless of fertilizer input; a meta-analysis. Eur J Plant Pathol 154(4):931–942. https://doi.org/10.1007/s10658-019-01711-4
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. Isme J 12(10):2339–2351. https://doi.org/10.1038/s41396-018-0171-4
Zhang L, Xu MG, Liu Y, Zhang FS, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210(3):1022–1032. https://doi.org/10.1111/nph.13838
Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hu L, Leung H (2000) Genetic diversity and disease control in rice. Nature 406(6797):718–722. https://doi.org/10.1038/35021046
Acknowledgements
This research was supported by National Key R & D Program of China (2017YFD0200200/2017YFD0200202) and National Natural Science Foundation of China (32002127). We acknowledge constructive comments by the editor and three reviewers on an earlier version of the manuscript.
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This research was supported by National Key R & D Program of China (2017YFD0200200/2017YFD0200202) and National Natural Science Foundation of China (32002127).
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C.L., J.Z., H.L., and F.Z. designed the study. C.L. collected the data. C.L., J.Z., E.H., and T.K. performed statistical analyses and led the writing and revision of the manuscript.
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Li, C., Li, H., Hoffland, E. et al. Common mycorrhizal networks asymmetrically improve chickpea N and P acquisition and cause overyielding by a millet/chickpea mixture. Plant Soil 472, 279–293 (2022). https://doi.org/10.1007/s11104-021-05232-0
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DOI: https://doi.org/10.1007/s11104-021-05232-0