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Physiological mechanisms behind endophytic fungus Phomopsis liquidambari-mediated symbiosis enhancement of peanut in a monocropping system

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Abstract

Background and aims

Fungal endophyte Phomopsis liquidambari B3 effectively increases nodule number and productivity of peanut when grown in a monoculturing system, but the underlying mechanisms are not well understood. Plant physiological status is the key mechanism that determines the legume-rhizobium interaction under stressful conditions. Therefore, this research aimed to study the physiological mechanisms behind the P. liquidambari-mediated monoculturing peanut nodulation enhancement.

Methods

Peanut-rhizobia symbiosis, plant defense enzyme activity in shoots and roots, photosynthetic activity and soluble sugar content in leaves, as well as the carbon metabolism-related enzyme activity and carbon metabolites content in nodules were measured after live P. liquidambari and P. liquidambari fragments treatment under continuous monoculturing condition.

Results

P. liquidambari instead of its fragments significantly enhanced nodule initiation, nodule development and nodule N2-fixation efficiency. Plants treated with live P. liquidambari showed higher leaf photosynthetic activity, soluble sugar accumulation, nodule carbohydrate catabolism activity and seed yield, whereas plant defense response was similar in endophyte and endophyte fragments treated plants.

Conclusion

Our results demonstrated that the improved efficiency of symbiosis in peanut continuous monoculturing system, induced by P. liquidambari, was likely linked to the improved plant aboveground nutritional status rather than to the induction of plant defense.

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References

  • Achatz B, von Ruden S, Andrade D, Neumann E, Pons-Kuhnemann J, Kogel KH, Franken P, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil 333:59–70

    Article  CAS  Google Scholar 

  • Akazawa T, Okamoto K (1980) Biosynthesis and metabolism of sucrose. In: Stumpf PK, Conn EE (eds) The biochemistry of plants, vol 3. Academic Press, New York, pp 199–220

    Google Scholar 

  • Anzuay MS, Ludueña LM, Angelini JG, Fabra A, Taurian T (2015) Beneficial effects of native phosphate solubilizing bacteria on peanut (Arachis hypogaea L) growth and phosphorus acquisition. Symbiosis 66(2):89–97

    Article  CAS  Google Scholar 

  • Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 171(12):1076–1090

    Article  CAS  PubMed  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681

    Article  CAS  PubMed  Google Scholar 

  • Baier MC, Barsch A, Küster H, Hohnjec N (2007) Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol 145(4):1600–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballhorn DJ, Younginger BS, Kautz S (2014) An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris. BMC Plant Biol 14(1):1

    Article  Google Scholar 

  • Barbour WM, Hattermann DR, Stacey G (1991) Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Environ Microbiol 57:2635–2639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowra BJ, Dilworth MJ (1981) Motility and chemotaxis towards sugars in Rhizobium leguminosarum. Microbiol 126:231–235

    Article  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chandler MR (1978) Some observations on infection of Arachis hypogaea L. by Rhizobium. J Exp Bot 29(3):749–755

    Article  Google Scholar 

  • Chen Y, Xie XG, Ren CG, Dai CC (2013) Degradation of N-heterocyclic indole by a novel endophytic fungus Phomopsis liquidambari. Bioresour Technol 129:568–574

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Fan JB, Du L, Xu H, Zhang QH, He YQ (2014) The application of phosphate solubilizing endophyte Pantoea dispersa triggers the microbial community in red acidic soil. Appl Soil Ecol 84:235–244

    Article  Google Scholar 

  • Chen F, Ren CG, Zhou T, Zhou T, Wei YJ, Dai CC (2016) A novel exopolysaccharide elicitor from endophytic fungus Gilmaniella sp. AL12 on volatile oils accumulation in Atractylodes lancea. Scientific reports 6:34735

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecol 69(1):10–16

    Article  Google Scholar 

  • Craig J, Barratt P, Tatge H, Déjardin A, Handley GCD, Barber L, Wang T, Hedley C, Martin C, Smith AM (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17(4):353–362

    Article  CAS  Google Scholar 

  • de Román M, Fernandez I, Wyatt T, Sahrawy M, Heil M, Pozo MJ (2011) Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. J Ecol 99(1):36–45

    Article  Google Scholar 

  • Dupont PY, Eaton CJ, Wargent JJ, Fechtner S, Solomon P, Schmid J, Day RC, Scott B, Cox MP (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208:1227–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013) Alleviation of salt stress of symbiotic Galega officinalis L. (goat's rue) by co-inoculation of rhizobium with root-colonizing pseudomonas. Plant Soil 369:453–465

    Article  CAS  Google Scholar 

  • Egamberdieva D, Jabborova D, Berg G (2016) Synergistic interactions between Bradyrhizobium japonicum and the endophyte Stenotrophomonas rhizophila and their effects on growth, and nodulation of soybean under salt stress. Plant Soil 405:35–45

    Article  CAS  Google Scholar 

  • el Zahar HF, Santaella C, Heulin T et al (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80

    Article  Google Scholar 

  • Fabra A, Castro S, Taurian T, Angelini J, Ibañez F, Dardanelli M, Tonelli M, Bianucci E, Valetti L (2010) Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Crit Rev Microbiol 36(3):179–194

    Article  CAS  PubMed  Google Scholar 

  • Faessel L, Nassr N, Lebeau T, Walter B (2010) Chemically-induced resistance on soybean inhibits nodulation and mycorrhization. Plant Soil 329:259–268

    Article  CAS  Google Scholar 

  • Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Int Compar Biol 42(2):360–368

    Article  Google Scholar 

  • Fox SL, O’Hara GW, Bräu L (2011) Enhanced nodulation and symbiotic effectiveness of Medicago truncatula when co-inoculated with Pseudomonas fluorescens WSM3457 and Ensifer (Sinorhizobium) medicae WSM419. Plant Soil 348:245–254

    Article  CAS  Google Scholar 

  • Foyer C, Spencer C (1986) The relationship between phosphate status and photosynthesis in leaves. Planta 167(3):369–375

    Article  CAS  PubMed  Google Scholar 

  • Freire JRJ (1984) Important limiting factors in soils for the Rhizobium legume symbiosis. In: Alexander M (ed) BNF ecology. Technology and Physiology. Plenum Press, New York, pp 51–74

    Google Scholar 

  • Frendo P, Matamoros MA, Alloing G, Becana M (2013) Thiol-based redox signaling in the nitrogen-fixing symbiosis. Front Plant Sci 4:376

    Article  PubMed  PubMed Central  Google Scholar 

  • Gordon AJ (1991) Enzyme distribution between the cortex and the infected region of soybean nodules. J Exp Bot 42(8):961–967

    Article  CAS  Google Scholar 

  • Gordon AJ, Ryle GJA, Mitchell DF, Powell DCE (1985) The flux of 14C-labelled photosynthate through soyabean root nodules during N2 fixation. J Exp Bot 36(5):756–769

    Article  CAS  Google Scholar 

  • Gordon AJ, Minchin FR, Skøt L, James CL (1997) Stress-induced declines in soybean N2 fixation are related to nodule sucrose synthase activity. Plant Physiol 114(3):937–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta KJ, Hebelstrup KH, Mur LAJ, Igamberdiev AU (2011) Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett 585(24):3843–3849

    Article  CAS  PubMed  Google Scholar 

  • Hentschel U, Steinert M, Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol 8:226–231

    Article  CAS  PubMed  Google Scholar 

  • Hwang S, Ray JD, Cregan PB, King CA, Davies MK, Purcell LC (2014) Genetics and mapping of quantitative traits for nodule number, weight, and size in soybean (Glycine max L.[Merr.]). Euphytica 195(3):419–434

    Article  CAS  Google Scholar 

  • Janczarek M, Rachwał K, Marzec A, Grzadziel J, Palusińska-Szysz M (2015) Signal molecules and cell-surface components involved in early stages of the legume–rhizobium interactions. Appl Soil Ecol 85:94–113

    Article  Google Scholar 

  • Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ Pollut 147(3):750–756

    Article  CAS  PubMed  Google Scholar 

  • Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52:103–122

    Google Scholar 

  • Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2015) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 35(1):62–74

    Article  CAS  PubMed  Google Scholar 

  • King CA, Purcell LC (2001) Soybean nodule size and relationship to nitrogen fixation response to water deficit. Crop Sci 41(4):1099–1107

    Article  Google Scholar 

  • Kouchi H, Fukai K, Katagiri H, Minamisawa K, Tajima S (1988) Isolation and enzymological characterization of infected and uninfected cell protoplasts from root nodules of Glycine max. Physiol Plant 73(3):327–334

    Article  CAS  Google Scholar 

  • Lafuente A, Pérez-Palacios P, Doukkali B, Molina-Sánchez J-Z, Caviedes MA, Rodríguez-Llorente PE (2015) Unraveling the effect of arsenic on the model Medicago–Ensifer interaction: a transcriptomic meta-analysis. New Phytol 205(1):255–272

    Article  CAS  PubMed  Google Scholar 

  • Larrainzar E, Gil-Quintana E, Seminario A, Arrese-lgor C, González EM (2014) Nodule carbohydrate catabolism is enhanced in the Medicago truncatula A17-Sinorhizobium medicae WSM419 symbiosis. Front Microbiol 5

  • Li X, Xu K (2014) Effects of exogenous hormones on leaf photosynthesis of Panax ginseng. Photosynthetica 52(1):152–156

    Article  CAS  Google Scholar 

  • Li XG, Ding CF, Zhang TL, Wang XX (2014) Fungal pathogen accumulation at the expense of plant-beneficial fungi as a consequence of consecutive peanut monoculturing. Soil Biol Biochem 72:11–18

    Article  CAS  Google Scholar 

  • Lin WY, Huang TK, Leong SJ, Chiou TJ (2014) Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J Exp Bot 65(7):1817–1827

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang N, Qiu M, Feng H, Vivanco JM, Shen Q, Zhang R (2014) Enhanced rhizosphere colonization of beneficial Bacillus amyloliquefaciens SQR9 by pathogen infection. FEMS Microbiol Lett 353(1):49–56

    Article  CAS  PubMed  Google Scholar 

  • Mathesius U (2008) Auxin: at the root of nodule development? Functional Plant Biol 35(8):651–668

    Article  CAS  Google Scholar 

  • Medeiros-Silva M, Franck WL, Borba MP, Pizzato SB, Strodtman KN, Emerich DW, Stacey G, Polacco JC, Carlini CR (2014) Soybean ureases, but not that of bradyrhizobium japonicum, are involved in the process of soybean root nodulation. J Agric Food Chem 62:3517–3524

    Article  CAS  PubMed  Google Scholar 

  • Minchin FR, Pate JS (1973) The carbon balance of a legume and the functional economy of its root nodules. J Exp Bot 24(2):259–271

    Article  CAS  Google Scholar 

  • Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Rahman K, Han T, Qin L (2013) Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J Exp Bot 64(18):5687–5694

    Article  CAS  PubMed  Google Scholar 

  • Moller L, Kessler KD, Steyn A, Valentine AJ, Botha A (2016) The role of Cryptococcus laurentii and mycorrhizal fungi in the nutritional physiology of Lupinus angustifolius L. hosting N2-fixing nodules. Plant Soil. doi:10.1007/s11104-016-2973-3

    Google Scholar 

  • Muñoz V, Ibáñez F, Tordable M, Megías M, Fabra A (2015) Role of reactive oxygen species generation and nod factors during the early symbiotic interaction between bradyrhizobia and peanut, a legume infected by crack entry. J Appl Microbiol 118(1):182–192

    Article  PubMed  Google Scholar 

  • Nasr Esfahani M, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2014) Approaches for enhancement of N2 fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions. Plant Biotechnol J 12(3):387–397

    Article  CAS  Google Scholar 

  • Ngwene B, Boukail S, Söllner L, Franken P, Andrade-Linares DR (2016) Phosphate utilization by the fungal root endophyte Piriformospora indica. Plant Soil 405:1–11

    Article  Google Scholar 

  • O’Hara GW, Dilworth MJ, Boonkerd N, Parkpian P (1988) Iron-deficiency specifically limits nodule development in peanut inoculated with Bradyrhizobium sp. New Phytol 108(1):51–57

    Article  Google Scholar 

  • Pate JS, Herridge DF (1978) Partitioning and utilization of net photosynthate in a nodulated annual legume. J Exp Bot 29(2):401–412

    Article  CAS  Google Scholar 

  • Peoples MB, Pate JS, Atkins CA, Bergersen FJ (1986) Nitrogen nutrition and xylem sap composition of peanut (Arachis hypogaea L. cv Virginia bunch). Plant Physiol 82:946–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peoples MB, Atkins CA, Pate JS, Chong K, Faizah AW, Suratmini P, Nurhayati DP, Bagnall DJ, Bergersen FJ (1991) Re-evaluation of the role of ureides in the xylem transport of nitrogen in Arachis species. Physiol Plant 83:560–567

    Article  CAS  Google Scholar 

  • Quilliam RS, DeLuca TH, Jones DL (2013) Biochar application reduces nodulation but increases nitrogenase activity in clover. Plant Soil 366:83–92

    Article  CAS  Google Scholar 

  • Ren A, Wei M, Yin L, Wu L, Zhou Y, Li X, Gao Y (2014) Benefits of a fungal endophyte in Leymus chinensis depend more on water than on nutrient availability. Environ Exp Bot 108:71–78

    Article  CAS  Google Scholar 

  • Samac DA, Graham MA (2007) Recent advances in legume-microbe interactions: recognition, defense response, and symbiosis from a genomic perspective. Plant Physiol 144:582–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulze J, Shi L, Blumenthal J, Samac DA, Gantt JS, Vance CP (1998) Inhibition of alfalfa root nodule phosphoenolpyruvate carboxylase through an antisense strategy impacts nitrogen fixation and plant growth. Phytochemistry 49(2):341–346

    Article  CAS  Google Scholar 

  • Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant-Microbe Interact 21(6):799–807

    Article  CAS  PubMed  Google Scholar 

  • Siddikee MA, Zereen MI, Li CF, Dai CC (2016) Endophytic fungus Phomopsis liquidambari and different doses of N-fertilizer alter microbial community structure and function in rhizosphere of rice. Sci Rep 6:32270

  • Streeter JG (1980) Carbohydrates in soybean nodules II. Distribution of compounds in seedlings during the onset of nitrogen fixation. Plant Physiol 66(3):471–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima S, Takane K, Nomura M, Kouchi H (2000) Symbiotic nitrogen fixation at the late stage of nodule formation in Lotus japonicus and other legume plants. J Plant Res 113(4):467–473

    Article  Google Scholar 

  • Tang C, Robson AD, Dilworth MJ (1990) The role of iron in nodulation and nitrogen fixation in Lupinus angustifolius L. New Phytol 114:173–182

    Article  CAS  Google Scholar 

  • van Dam NM, Heil M (2011) Multitrophic interactions below and above ground: en route to the next level. J Ecol 99(1):77–88

    Article  Google Scholar 

  • Vance CP (2008) Carbon and nitrogen metabolism in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Netherlands, pp 293–320

  • Vayssières A, Pěnčík A, Felten J, Kohler A, Ljung K, Martin F, Legué V (2015) Development of the poplar-Laccaria bicolor Ectomycorrhiza modifies root auxin metabolism, signaling, and response. Plant Physiol 169(1):890–902

    Article  PubMed  PubMed Central  Google Scholar 

  • Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195(2):306–320

    Article  CAS  PubMed  Google Scholar 

  • Walters D, Heil M (2007) Cost and trade-offs associated with induced resistance. Physiol Mol Plant Path 71:3–17

    Article  CAS  Google Scholar 

  • Walters D, Newton A, Lyon G (2005) Induced resistance: helping plants to help themselves. Biologist 52:28–33

    Google Scholar 

  • Wang MZ, Chen XN (2005) Obstacle and countermeasure of sustainable high yield for peanut in low-hilly red soil region. J Peanut Sci (in Chinese) 34:17–22

    CAS  Google Scholar 

  • Wang HW, Wang XX, Lü LX, Xiao Y, Dai CC (2012) Effects of applying endophytic fungi on the soil biological characteristics and enzyme activities under continuous cropped peanut. China J Appl Ecol 23:2693–2700

    CAS  Google Scholar 

  • Wang HW, Dai CC, Zhu H, Wang XX (2014) Survival of a novel endophytic fungus Phomopsis liquidambari B3 in the indole contaminated soil detected by real-time PCR and its effects on the indigenous microbial community. Microbiol Res 169:881–887

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Wu C, Cheng Z, Meng H (2015a) Growth and physiological changes in continuously cropped eggplant (Solanum melongena L.) upon relay intercropping with garlic (Allium sativum L.) Frontiers Plant Sci 6:262

    Google Scholar 

  • Wang XM, Yang B, Wang HW, Yang T, Ren CG, Zheng HL, Dai CC (2015b) Consequences of antagonistic interactions between endophytic fungus and bacterium on plant growth and defense responses in Atractylodes lancea. J Basic Microbiol 55(5):659–670

    Article  CAS  PubMed  Google Scholar 

  • Waqas M, Khan AL, Hamayun M, Shahzad R, Kang SM, Kim JG, Lee IJ (2015) Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus. J Plant Interact 10(1):280–287

    Article  CAS  Google Scholar 

  • Xia C, Li N, Zhang X, Feng Y, Christensen MJ, Nan Z (2016) An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol 22:26–34

    Article  Google Scholar 

  • Xiao X, Cheng Z, Meng H et al (2012) Intercropping with garlic alleviated continuous cropping obstacle of cucumber in plastic tunnel. Acta Agriculturae Scandinavica, Section B–Soil & Plant Science 62(8):696–705

    Article  Google Scholar 

  • Xie XG, Dai CC (2015) Degradation of a model pollutant ferulic acid by the endophytic fungus Phomopsis liquidambari. Bioresour Technol 179:35–42

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Wang XM, Ma HY, Jia Y, Xia L, Dai CC (2014) Effects of the fungal endophyte Phomopsis liquidambari on nitrogen uptake and metabolism in rice. Plant Growth Regul 82:172–182

    CAS  Google Scholar 

  • Yang B, Wang XM, Ma HY, Yang T, Jia Y, Dai CC (2015) Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front in Microbiol 6:982

    Google Scholar 

  • Yuan ZL, Dai CC, Shi Y, Wang AQ (2004) Study of the mechanism of a strain of endophytic fungi’s stimulation the growth of rice. Jiangsu J Agric Sci 2:10–13

    Google Scholar 

  • Zhang F, Meng X, Yang X, Ran W, Shen Q (2014) Quantification and role of organic acids in cucumber root exudates in Trichoderma harzianum T-E5 colonization. Plant Physiol Biochem 83:250–257

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Wang HW, Wang XX, Xie XX, Siddikee MA, Xu RS, Dai CC (2016) Enhanced nodulation of peanut when co-inoculated with fungal endophyte Phomopsis liquidambari and bradyrhizobium. Plant Physiol Biochem 98:1–11

    Article  PubMed  Google Scholar 

  • Zhao J (2015) Flavonoid transport mechanisms: how to go, and with whom. Trends Plant Sci 20(9):576–585

    Article  CAS  PubMed  Google Scholar 

  • Zheng C, Ji B, Zhang J, Zhang F, Bever JD (2015) Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. New Phytol 205:361–368

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the National Natural Science Foundation of China (NSFC NO 31370507), the Ph.D. Programs Foundation of Ministry of Education of China (No. 20133207110001), the Major Natural Science Research Programs of Jiangsu Higher Education Institutions (No. 13KJA180003), a project funded by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions of China, Graduate Education innovation Project of Jiangsu Province (KYLX_0711), and funded by the Doctor Breeding Project of Nanjing Normal University (No. 1812000006317). The authors express their great thanks to anonymous reviewers and editorial staff for their time and attention.

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  1. Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University, Jiangsu Province, China

    Wei Zhang, Zhen Yang, Siddikee Md Ashaduzzaman, Meng-Juan Kong, Li-Ying Lu, Jing-Xuan Shen & Chuan-Chao Dai

  2. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Jiangsu Province, China

    Xing-Xiang Wang

  3. Jiangxi Key Laboratory of Ecological Research of Red Soil, Experimental Station of Red Soil, Chinese Academy of Sciences, Jiangxi Province, China

    Xing-Xiang Wang

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  1. Wei Zhang
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Zhang, W., Wang, XX., Yang, Z. et al. Physiological mechanisms behind endophytic fungus Phomopsis liquidambari-mediated symbiosis enhancement of peanut in a monocropping system. Plant Soil 416, 325–342 (2017). https://doi.org/10.1007/s11104-017-3219-8

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