[en] Intercropping achieved through agroforestry is increasingly being recognized as a sustainable form of land use. In agroforestry, the roots of trees and crops are intermingled, and their interactions and the production of exudates alter the soil environment and soil microbial community. Although tree-crop interactions vary depending on the stand age of the trees, how stand age affects beneficial microorganisms, including arbuscular mycorrhizal fungi (AMF), and whether changes in soil microorganisms feed back on crop growth in agroforestry systems are unknown. We therefore conducted a long-term field study to compare changes in the soil microbial and AMF communities in a jujube/wheat agroforestry system containing trees of different stand ages: 3-year-old jujube, 8-year-old jujube, and 13-year-old jujube. Our results showed that by changing soil moisture and available phosphorus content, the stand age of the trees had a significant effect on the soil microbial and AMF communities. Soil moisture altered the composition of soil bacteria, in particular the proportions of Gram-positive and Gram-negative species, and available phosphorus had significant effects on the AMF community. A network analysis showed that older stands of trees reduced both AMF diversity and network complexity. An ordinary least squares regression analysis indicated that AMF diversity, network complexity, and stability contributed to wheat yield. Finally, structural equation modeling showed that changes in edaphic factors induced by tree age brought about significant variation in the soil microbial and AMF communities, in turn, affecting crop growth. Our study highlights the crucial roles of soil microorganisms, in particular AMF, in supporting plant growth in agroforestry systems as well as the need to consider stand age in the establishment of these systems.
Disciplines :
Agriculture & agronomy
Author, co-author :
Qiao, Xu ✱; Peking Union Medical College, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences, Beijing, China ; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Sun, Tao ✱; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China ; College of Water Conservancy and Civil Engineering, Xinjiang Agricultural University, Urumqi, China ; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China
Lei, Junjie; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Xiao, Li; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Xue, Lihua; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China
Zhang, Heng; Key Laboratory of Desert-Oasis Crop Physiology, Ecology and Cultivation, MOARA/Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi, China ; College of Water Conservancy and Civil Engineering, Xinjiang Agricultural University, Urumqi, China
Jia, Jiyu; Peking Union Medical College, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences, Beijing, China ; Key Laboratory of Plant-Soil Interactions, College of Resources and Environmental Sciences, Ministry of Education, National Academy of Agriculture Green Development, China Agricultural University, Beijing, China
Bei, Shuikuan; Peking Union Medical College, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences, Beijing, China ; Key Laboratory of Plant-Soil Interactions, College of Resources and Environmental Sciences, Ministry of Education, National Academy of Agriculture Green Development, China Agricultural University, Beijing, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Arbuscular mycorrhizal fungi contribute to wheat yield in an agroforestry system with different tree ages.
NSCF - National Natural Science Foundation of China
Funding text :
We are grateful for the support from the Extension Centre of Agricultural Technology in Zepu County, Kashi Prefecture, Xinjiang. We also would like to thank the reviewers and the editors for their helpful comments.This work was funded by the Key Cultivation Project of Scientific and Technological Innovation of Xinjiang Academy of Agricultural Sciences (xjkcpy-003), Key Research and Development Projects of Xinjiang (2021B02002), National Natural Science Foundation of China (Grant Nos. 31560587, 32160521, 32060433), The central government guides local funds for science and technology development (2060503), and the Modern Agricultural Industry Technology System (CARS-03-49).
Allison S. D. Martiny J. B. (2008). Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U. S. 105, 11512–11519. doi: 10.1073/pnas.0801925105
Araujo A. S. F. Leite L. F. C. Iwata B. F. Lira M. A. Xavier G. R. Figueiredo M. V. B. (2012). Microbiological process in agroforestry systems. A review. Agron. Sustain. Dev. 32, 215–226. doi: 10.1007/s13593-011-0026-0
Baah-Acheamfour M. Carlyle C. N. Bork E. W. Chang S. X. (2014). Trees increase soil carbon and its stability in three agroforestry systems in Central Alberta, Canada. Forest Ecol. Manag. 328, 131–139. doi: 10.1016/j.foreco.2014.05.031
Bagyaraj D. J. Thilagar G. Ravisha C. Kushalappa C. G. Krishnamurthy K. N. Vaast P. (2015). Below ground microbial diversity as influenced by coffee agroforestry systems in the Western Ghats, India. Agric. Ecosyst. Environ. 202, 198–202. doi: 10.1016/j.agee.2015.01.015
Bahadur A. Batool A. Nasir F. Jiang S. Mingsen Q. Zhang Q. et al. (2019). Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int. J. Mol. Sci. 20:4199. doi: 10.3390/ijms20174199, PMID: 31461957
Barrios E. (2007). Soil biota, ecosystem services and land productivity. Ecol. Econ. 64, 269–285. doi: 10.1016/j.ecolecon.2007.03.004
Bastida F. Selevsek N. Torres I. F. Hernández T. García C. (2015). Soil restoration with organic amendments: linking cellular functionality and ecosystem processes. Sci. Rep. 5:15550. doi: 10.1038/srep15550, PMID: 26503516
Begum N. Qin C. Ahanger M. A. Raza S. Khan M. I. Ashraf M. et al. (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front. Plant Sci. 10:1068. doi: 10.3389/fpls.2019.01068, PMID: 31608075
Bell C. McIntyre N. Cox S. Tissue D. Zak J. (2008). Soil microbial responses to temporal variations of moisture and temperature in a Chihuahuan Desert grassland. Microb. Ecol. 56, 153–167. doi: 10.1007/s00248-007-9333-z, PMID: 18246293
Beule L. Lehtsaar E. Corre M. D. Schmidt M. Veldkamp E. Karlovsky P. (2020). Poplar rows in temperate agroforestry croplands promote bacteria, fungi, and denitrification genes in soils. Front. Microbiol. 10:3108. doi: 10.3389/fmicb.2019.03108, PMID: 32038551
Bever J. D. (2003). Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 157, 465–473. doi: 10.1046/j.1469-8137.2003.00714.x, PMID: 33873396
Boer W. De Folman L. B. Summerbell R. C. Boddy L. (2005). Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29, 795–811. doi: 10.1016/j.femsre.2004.11.005, PMID: 16102603
Bryla D. R. Eissenstat D. M. (2005). “Respiratory costs of mycorrhizal associations,” in Plant Respiration. eds. Lambers H. Ribas-Carbo M. (Dordrecht: Springer), 207–224.
Campos C. Carvalho M. Brígido C. Goss M. J. Nobre T. (2018). Symbiosis specificity of the preceding host plant can dominate but not obliterate the association between wheat and its arbuscular mycorrhizal fungal partners. Front. Microbiol. 9:2920. doi: 10.3389/fmicb.2018.02920, PMID: 30542338
Caravaca F. Rodriguez-Caballero G. Campoy M. Sanleandro P. M. Roldán A. (2020). The invasion of semiarid Mediterranean sites by Nicotiana glauca mediates temporary changes in mycorrhizal associations and a permanent decrease in rhizosphere activity. Plant Soil 450, 217–229. doi: 10.1007/s11104-020-04497-1
Cheng X. F. Wu H. H. Zou Y. N. Wu Q. S. Kuča K. (2021). Mycorrhizal response strategies of trifoliate orange under well-watered, salt stress, and waterlogging stress by regulating leaf aquaporin expression. Plant Physiol. Biochem. 162, 27–35. doi: 10.1016/j.plaphy.2021.02.026, PMID: 33662869
Compant S. Clément C. Sessitsch A. (2010). Plant growth-promoting bacteria in the rhizo- and endo-sphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669–678. doi: 10.1016/j.soilbio.2009.11.024
Csardi G. Nepusz T. (2006). The igraph software package for complex network research. InterJ. Complex Syst. 1695, 1–9. Available at: https://igraph.org
De Vries F. T. Shade A. (2013). Control son soil microbial community stability under climate change. Front. Microbiol. 4, 1–16. doi: 10.3389/fmicb.2013.00265
Deepika S. Kothamasi D. (2015). Soil moisture—a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25, 67–75. doi: 10.1007/s00572-014-0596-1, PMID: 25085217
Dollinger J. Jose S. (2018). Agroforestry for soil health. Agrofor. Syst. 92, 213–219. doi: 10.1007/s10457-018-0223-9
Duc N. H. Csintalan Z. Posta K. (2018). Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol. Biochem. 132, 297–307. doi: 10.1016/j.plaphy.2018.09.011, PMID: 30245343
Duchene O. Vian J. F. Celette F. (2017). Intercropping with legume for agroecological cropping systems: complementarity and facilitation processes and the importance of soil microorganisms. A review. Agric. Ecosyst. Environ. 240, 148–161. doi: 10.1016/j.agee.2017.02.019
Fanin N. Kardol P. Farrell M. Nilsson M. C. Gundale M. J. Wardle D. A. (2019). The ratio of gram-positive to gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biol. Biochem. 128, 111–114. doi: 10.1016/j.soilbio.2018.10.010
Fentahun M. Hager H. (2010). Integration of indigenous wild woody perennial edible fruit bearing species in the agricultural landscapes of Amhara region, Ethiopia. Agrofor. Syst. 78, 79–95. doi: 10.1007/s10457-009-9239-5
Frostegård Å. Tunlid A. Bååth E. (2011). Use and misuse of PLFA measurements in soils. Soil Biol. Biochem. 43, 1621–1625. doi: 10.1016/j.soilbio.2010.11.021
Gao P. Zheng X. Wang L. Liu B. Zhang S. (2019). Changes in the soil bacterial community in a chronosequence of temperate walnut-based intercropping systems. Forests 10:299. doi: 10.3390/f10040299
Giovannetti M. Mosse B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500. doi: 10.1111/j.1469-8137.1980.tb04556.x
Grace J. B. Keeley J. E. (2006). A structural equation model analysis of postfire plant diversity in California shrublands. Ecol. Appl. 16, 503–514. doi: 10.1890/1051-0761(2006)016[0503:ASEMAO]2.0.CO;2, PMID: 16711040
Guzman A. Montes M. Hutchins L. DeLaCerda G. Yang P. Kakouridis A. et al. (2021). Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol. 231, 447–459. doi: 10.1111/nph.17306, PMID: 33638170
Hailemariam M. Birhane E. Asfaw Z. Zewdie S. (2013). Arbuscular mycorrhizal association of indigenous agroforestry tree species and their infective potential with maize in the rift valley, Ethiopia. Agrofor. Syst. 87, 1261–1272. doi: 10.1007/s10457-013-9634-9
Herrmann L. Lesueur D. Bräu L. Davison J. Jairus T. Robain H. et al. (2016). Diversity of root-associated arbuscular mycorrhizal fungal communities in a rubber tree plantation chronosequence in Northeast Thailand. Mycorrhiza 26, 863–877. doi: 10.1007/s00572-016-0720-5, PMID: 27448680
Hugerth L. W. Andersson A. F. (2017). Analysing microbial community composition through amplicon sequencing: from sampling to hypothesis testing. Front. Microbiol. 8:1561. doi: 10.3389/fmicb.2017.01561, PMID: 28928718
Hutchins D. A. Jansson J. K. Remais J. V. Rich V. I. Singh B. K. Trivedi P. (2019). Climate change microbiology—problems and perspectives. Nat. Rev. Microbiol. 17, 391–396. doi: 10.1038/s41579-019-0178-5, PMID: 31092905
Jeffries P. Gianinazzi S. Perotto S. Turnau K. Barea J. M. (2003). The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 37, 1–16. doi: 10.1007/s00374-002-0546-5
Jing Y. Wang Y. Liu S. Zhang X. Wang Q. Liu K. et al. (2019). Interactive effects of soil warming, throughfall reduction, and root exclusion on soil microbial community and residues in warm-temperate oak forests. Appl. Soil Ecol. 142, 52–58. doi: 10.1016/j.apsoil.2019.05.020
Jurburg S. D. Nunes I. Stegen J. C. Le Roux X. Priemé A. Sørensen S. J. et al. (2017). Autogenic succession and deterministic recovery following disturbance in soil bacterial communities. Sci. Rep. 7, 1–11. doi: 10.1038/srep45691
Kaiser M. Kleber M. Berhe A. A. (2015). How air-drying and rewetting modify soil organic matter characteristics: an assessment to improve data interpretation and inference. Soil Biol. Biochem. 80, 324–340. doi: 10.1016/j.soilbio.2014.10.018
Kempf B. Bremer E. (1998). Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319–330. doi: 10.1007/s002030050649, PMID: 9818351
Kiers E. T. Duhamel M. Beesetty Y. Mensah J. A. Franken O. Verbruggen E. et al. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882. doi: 10.1126/science.1208473, PMID: 21836016
Knegt B. Jansa J. Franken O. Engelmoer D. J. P. Werner G. D. A. Bücking H. et al. (2016). Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol. 20, 233–240. doi: 10.1016/j.funeco.2014.09.011
Köster K. Berninger F. Lindén A. Köster E. Pumpanen J. (2014). Recovery in fungal biomass is related to decrease in soil organic matter turnover time in a boreal fir chronosequence. Geoderma 235-236, 74–82. doi: 10.1016/j.geoderma.2014.07.001
Li D. Liu C. M. Luo R. Sadakane K. Lam T. W. (2015). MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676. doi: 10.1093/bioinformatics/btv033, PMID: 25609793
Liu C. Jin Y. Hu Y. Tang J. Xiong Q. Xu M. et al. (2019). Drivers of soil bacterial community structure and diversity in tropical agroforestry systems. Agric. Ecosyst. Environ. 278, 24–34. doi: 10.1016/j.agee.2019.03.015
Malamy J. E. (2005). Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28, 67–77. doi: 10.1111/j.1365-3040.2005.01306.x, PMID: 16021787
Marro N. Grilli G. Soteras F. Caccia M. Longo S. Cofré N. et al. (2022). The effects of arbuscular mycorrhizal fungal species and taxonomic groups on stressed and unstressed plants: a global meta-analysis. New Phytol. 235, 320–332. doi: 10.1111/nph.18102, PMID: 35302658
Mason P. A. Wilson J. (1994). “Harnessing symbiotic associations: vesicular-arbuscular mycorrhizas,” in Tropical Trees: The Potential for Domestication and the Rebuilding of Forest Resources. eds. Leakey R. R. B. Newton A. C. (London: HMSO), 165–175.
Menezes K. M. Silva D. K. Queiroz M. A. Félix W. P. Yano-Melo A. M. (2016). Arbuscular mycorrhizal fungal communities in buffelgrass pasture under intercropping and shading systems in Brazilian semiarid conditions. Agric. Ecosyst. Environ. 230, 55–67. doi: 10.1016/j.agee.2016.05.024
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. 6:339. doi: 10.3389/fpls.2015.00339
Oksanen J. Blanchet F. G. Friendly M. Kindt R. Legendre P. McGlinn D. et al. (2019). Vegan: Community ecology package, version 2.5–6.
Oren A. (2008). Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst. 4, 2–13. doi: 10.1186/1746-1448-4-2
Page A. Miller R. Keeney D. (1982). Methods of Soil Analysis, Part 2. Chemical and Microbiological Properties. Madison, WI, American Society of Agronomy, Inc., Soil Science Society of America.
Peerawat M. Blaud A. Trap J. Chevallier T. Alonso P. Gay F. et al. (2018). Rubber plantation ageing controls soil biodiversity after land conversion from cassava. Agric. Ecosyst. Environ. 257, 92–102. doi: 10.1016/j.agee.2018.01.034
Philippot L. Raaijmakers J. M. Lemanceau P. van Der Putten W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799. doi: 10.1038/nrmicro3109, PMID: 24056930
Piton G. Foulquier A. Martinez-García L. B. Legay N. Arnoldi C. Brussaard L. et al. (2021). Resistance–recovery trade-off of soil microbial communities under altered rain regimes: an experimental test across European agroecosystems. J. Appl. Ecol. 58, 406–418. doi: 10.1111/1365-2664.13774
R Core Team (2020). R: a language and environment for statistical computing.
Radhakrishnan S. Varadharajan M. (2016). Status of microbial diversity in agroforestry systems in Tamil Nadu, India. J. Basic Microbiol. 56, 662–669. doi: 10.1002/jobm.201500639, PMID: 26924716
Remison S. U. Snaydon R. W. (1980). A comparison of root competition and shoot competition between Dactylis glomerata and Holcus lanatus. Grass Forage Sci. 35, 183–187. doi: 10.1111/j.1365-2494.1980.tb01510.x
Robeson M. S. King A. J. Freeman K. R. Birky C. W. Martin A. P. Schmidt S. K. (2011). Soil rotifer communities are extremely diverse globally but spatially autocorrelated locally. Proc. Natl. Acad. Sci. U. S. 108, 4406–4410. doi: 10.1073/pnas.1012678108
Rodrigues J. L. M. Pellizari V. H. Mueller R. Baek K. Da Jesus E. C. Paula F. S. et al. (2013). Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 110, 988–993. doi: 10.1073/pnas.1220608110, PMID: 23271810
Sato K. Suyama Y. Saito M. Sugawara K. (2005). A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl. Sci. 51, 179–181. doi: 10.1111/j.1744-697X.2005.00023.x
Schimel J. Balser T. C. Wallenstein M. (2007). Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394. doi: 10.1890/06-0219, PMID: 17601131
Sheng M. Chen X. Zhang X. Hamel C. Cui X. Chen J. et al. (2017). Changes in arbuscular mycorrhizal fungal attributes along a chronosequence of black locust (Robinia pseudoacacia) plantations can be attributed to the plantation-induced variation in soil properties. Sci. Total Environ. 599-600, 273–283. doi: 10.1016/j.scitotenv.2017.04.199
Shukla A. Kumar A. Jha A. Chaturvedi O. P. Prasad R. Gupta A. (2009). Effects of shade on arbuscular mycorrhizal colonization and growth of crops and tree seedlings in Central India. Agrofor. Syst. 76, 95–109. doi: 10.1007/s10457-008-9182-x
Simon L. Lalonde M. Bruns T. D. (1992). Specific amplification of 18S fungal ribosomal genes from vesicular arbuscular endomycorrhizal fungi colonizing roots. Appl. Environ. Microbiol. 58, 291–295. doi: 10.1128/aem.58.1.291-295.1992, PMID: 1339260
Souza T. (2015). “Glomeromycota classification,” in Handbook of Arbuscular Mycorrhizal Fungi (Cham: Springer International Publishing), 87–128.
Sýkorová Z. Ineichen K. Wiemken A. Redecker D. (2007). The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18, 1–14. doi: 10.1007/s00572-007-0147-0, PMID: 17879101
Tamburini G. Bommarco R. Wanger T. C. Kremen C. van der Heijden M. G. Liebman M. et al. (2020). Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6:eaba1715. doi: 10.1126/sciadv.aba1715, PMID: 33148637
Torrecillas E. Alguacil M. M. Roldan A. (2012). Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl. Environ. Microbiol. 78, 6180–6186. doi: 10.1128/AEM.01287-12, PMID: 22752164
Tscharntke T. Clough Y. Bhagwat S. A. Buchori D. Faust H. Hertel D. et al. (2011). Multifunctional shade-tree management in tropical agroforestry landscapes–a review. J. Appl. Ecol. 48, 619–629. doi: 10.1111/j.1365-2664.2010.01939.x
Turrini A. Avio L. Giovannetti M. Agnolucci M. (2018). Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front. Plant Sci. 9:1407. doi: 10.3389/fpls.2018.01407, PMID: 30319670
van Dam N. M. Bouwmeester H. J. (2016). Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci. 21, 256–265. doi: 10.1016/j.tplants.2016.01.008, PMID: 26832948
van Tuinen D. Tranchand E. Hirissou F. Wipf D. Courty P. E. (2020). Carbon partitioning in a walnut-maize agroforestry system through arbuscular mycorrhizal fungi. Rhizosphere 15:100230. doi: 10.1016/j.rhisph.2020.100230
Verbruggen E. Van Der HEIJDEN M. G. Weedon J. T. Kowalchuk G. A. Röling W. F. (2012). Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol. Ecol. 21, 2341–2353. doi: 10.1111/j.1365-294X.2012.05534.x, PMID: 22439851
Veresoglou S. D. Caruso T. Rillig M. C. (2013). Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant Soil 368, 507–518. doi: 10.1007/s11104-012-1531-x
Ward P. R. Dunin F. X. Micin S. F. (2002). Water use and root growth by annual and perennial pastures and subsequent crops in a phase rotation. Agric. Water Manag. 53, 83–97. doi: 10.1016/S0378-3774(01)00157-3
Wei Z. Gu Y. Friman V. P. Kowalchuk G. A. Xu Y. Shen Q. et al. (2019). Initial soil microbiome composition and functioning predetermine future plant health. Sci. Adv. 5:eaaw0759. doi: 10.1126/sciadv.aaw0759, PMID: 31579818
White T. J. Bruns T. Lee S. J. W. T. Taylor J. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR Protocols: A Guide to Methods and Applications. eds. Innis M. A. Gelfand D. H. Sninsky J. J. White T. J. (San Diego, CA: Academic Press), 315e322.
Wipf D. Krajinski F. van Tuinen D. Recorbet G. Courty P. E. (2019). Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytol. 223, 1127–1142. doi: 10.1111/nph.15775, PMID: 30843207
Yao H. Jiao X. Wu F. (2006). Effects of continuous cucumber cropping and alternative rotations under protected cultivation on soil microbial community diversity. Plant Soil 284, 195–203. doi: 10.1007/s11104-006-0023-2
Yao Z. Xing J. Gu H. Wang H. Wu J. Xu J. et al. (2016). Development of microbial community structure in vegetable-growing soils from open-field to plastic-greenhouse cultivation based on the PLFA analysis. J. Soils Sediments 16, 2041–2049. doi: 10.1007/s11368-016-1397-2
Zhang D. Zhang L. Liu J. Han S. Wang Q. Evers J. et al. (2014). Plant density affects light interception and yield in cotton grown as companion crop in young jujube plantations. Field Crops Res. 169, 132–139. doi: 10.1016/j.fcr.2014.09.001
Zhang Z. Zhang J. Xu G. Zhou L. Li Y. (2019b). b. Arbuscular mycorrhizal fungi improve the growth and drought tolerance of Zenia insignis seedlings under drought stress. New For. 50, 593–604. doi: 10.1007/s11056-018-9681-1
Zhang Y. Zheng N. Wang J. Yao H. Qiu Q. Chapman S. J. (2019a). a. High turnover rate of free phospholipids in soil confirms the classic hypothesis of PLFA methodology. Soil Biol. Biochem. 135, 323–330. doi: 10.1016/j.soilbio.2019.05.023
Zhu Y. G. Miller R. M. (2003). Carbon cycling by arbuscular mycorrhizal fungi in soil–plant systems. Trends Plant Sci. 8, 407–409. doi: 10.1016/S1360-1385(03)00184-5, PMID: 13678905