Abstract
Replant failure has threatened the production of Sanqi ginseng (Panax notoginseng) mainly due to the accumulation of soil-borne pathogens and allelochemicals. Reductive soil disinfestation (RSD) is an effective practice used to eliminate soil-borne pathogens; however, the potential impact of RSD on the degradation of allelochemicals and the growth of replant Sanqi ginseng seedlings remain poorly understood. In this study, RSD was conducted on a Sanqi ginseng monoculture system (SGMS) and a maize-Sanqi ginseng system (MSGS), defined as SGMS_RSD and MSGS_RSD, respectively. The aim was to investigate the impact of RSD on allelochemicals, soil microbiomes, and survival rates of replant seedlings. Both short-term maize planting and RSD treatment significantly degraded the ginsenosides in Sanqi ginseng–cultivated soils, with the degradation rate being higher in the RSD treatment. The population of Fusarium oxysporum and the relative abundance of genus Fusarium were dramatically suppressed by RSD treatment. Furthermore, the RSD treatment, but not maize planting, markedly alleviated the replant failure of Sanqi ginseng, with the seedling survival rate being 52.7–70.7% 6 months after transplanting. Interestingly, RSD followed by short-term maize planting promoted microbial activity restoration, ginsenoside degradation, and ultimately alleviated the replant failure much better than RSD treatment alone (70.7% vs. 52.7%). Collectively, these results indicate that RSD treatment could considerably reduce the obstacles and might also act as a potential agriculture regime for overcoming the replant failure of Sanqi ginseng. Additional practices, such as crop rotation, beneficial microorganism inoculation, etc. may also still be needed to ensure the long-term efficacy of seedling survival.
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References
Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33:943–951. https://doi.org/10.1016/S0038-0717(00)00244-3
Anderson MJ (2005) Permutational multivariate analysis of variance. Dep Stat Univ Auckland, Auckland 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ (2000) Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology 90:253–259. https://doi.org/10.1094/PHYTO.2000.90.3.253
Brinckmann JA (2013) Emerging importance of geographical indications and designations of origin—authenticating geo-authentic botanicals and implications for phytotherapy. Phytother Res 27:1581–1587. https://doi.org/10.1002/ptr.4912
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Chen Y, Wang HW, Li L, Dai CC (2013) The potential application of the endophyte Phomopsis liquidambari to the ecological remediation of long-term cropping soil. Appl Soil Ecol 67:20–26. https://doi.org/10.1016/j.apsoil.2013.02.004
Choi JR, Hong SW, Kim Y, Jiang SE, Kim NJ, Han MJ, Kim DH (2011) Metabolic activities of ginseng and its constituents, ginsenoside Rb1 and Rg1, by human intestinal microflora. J Ginseng Res 35:301–307. https://doi.org/10.5142/jgr.2011.35.3.301
Christensen LP (2008) Ginsenosides: chemistry, biosynthesis, analysis, and potential health effects. Adv Food Nutr Res 55:1–99. https://doi.org/10.1016/S1043-4526(08)00401-4
Cui CH, Kim JK, Kim SC, Im WT (2014) Characterization of a ginsenoside-transforming β-glucosidase from Paenibacillus mucilaginosus and its application for enhanced production of minor ginsenoside F2. PLoS One 9(1):e85727. https://doi.org/10.1371/journal.pone.0085727
Dong LL, Jiang X, Feng G, Li X, Chen S (2016) Soil bacterial and fungal community dynamics in relation to Panax notoginseng death rate in a continuous cropping system. Sci Rep 6:31802. https://doi.org/10.1038/srep31802
Dong LL, Xu J, Li Y, Fang HL, Niu WH, Li XW, Zhang YJ, Ding WL, Chen S (2018a) Manipulation of microbial community in the rhizosphere alleviates the replanting issues in Panax ginseng. Soil Biol Biochem 125:64–74. https://doi.org/10.1016/j.soilbio.2018.06.028
Dong LL, Xu J, Zhang LJ, Cheng RY, Wei GF, Su H, Yang J, Qian J, Xu R, Chen S (2018b) Rhizospheric microbial communities are driven by Panax ginseng at different growth stages and biocontrol bacteria alleviates replanting mortality. Acta Pharm Sin B 8:272–282. https://doi.org/10.1016/j.apsb.2017.12.011
Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270. https://doi.org/10.1146/annurev.phyto.42.012604.135455
Guo HB, Cui XM, An N, Cai GP (2010) Sanchi ginseng (Panax notoginseng (Burkill) F. H. Chen) in China: distribution, cultivation and variations. Genet Resour Crop Evol 57:453–460. https://doi.org/10.1007/s10722-010-9531-2
Häggblom M (1990) Mechanisms of bacterial degradation and transformation of chlorinated monoaromatic compounds. J Basic Microbiol 30:115–141. https://doi.org/10.1002/jobm.3620300214
Hartmann A, Schmid M, Tuinen DV, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257. https://doi.org/10.1007/s11104-008-9814-y
Huang XQ, Wen T, Zhang JB, Meng L, Zhu TB, Liu LL, Cai ZC (2015a) Control of soil-borne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J Plant Pathol 143:223–235. https://doi.org/10.1007/s10658-015-0676-x
Huang XQ, Liu LQ, Wen T, Zhu R, Zhang JB, Cai ZC (2015b) Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f.sp. cubense infected soil during and after reductive soil disinfestation. Microbiol Res 181:33–42. https://doi.org/10.1016/j.micres.2015.08.004
Huang XQ, Liu LL, Wen T, Zhang JB, Wang F, Cai ZC (2016a) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol 100:5581–5593. https://doi.org/10.1007/s00253-016-7362-6
Huang XQ, Liu LL, Wen T, Zhang JB, Shen QR, Cai ZC (2016b) Reductive soil disinfestations combined or not with Trichoderma for the treatment of a degraded and Rhizoctonia solani infested greenhouse soil. Sci Hortic 206:51–61. https://doi.org/10.1016/j.scienta.2016.04.033
Inderjit (2005) Soil microorganisms: an important determinant of allelopathic activity. Plant Soil 274:227–236. https://doi.org/10.1007/s11104-004-0159-x
Jiao XL, Bi W, Li M, Luo Y, Gao WW (2011) Dynamic response of ginsenosides in American ginseng to root fungal pathogens. Plant Soil 339:317–327. https://doi.org/10.1007/s11104-010-0580-2
Jiao XL, Lu XH, Chen AJ, Luo Y, Hao JJ, Gao WW (2015) Effects of Fusarium solani and F. oxysporum infection on the metabolism of ginsenosides in American ginseng roots. Molecules 20:10535–10552. https://doi.org/10.3390/molecules200610535
Kim KA, Jung IH, Park SH, Ahn YT, Huh CS, Kim DH (2013) Comparative analysis of the gut microbiota in people with different levels of ginsenoside Rb1 degradation to compound K. PLoS One 8:e62409. https://doi.org/10.1371/journal.pone.0062409
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. https://doi.org/10.1111/mec.12481
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Lamers JG, Mazzola M, Rosskopf EN, Kokalis-Burelle N, Momma N, Butler DM, Kobara Y (2014) Anaerobic soil disinfestation for soil borne disease control in strawberry and vegetable systems: current knowledge and future directions. Acta Hortic 1044:165–175. https://doi.org/10.17660/ActaHortic.2014.1044.20
Lee HJ, Cho GY, Chung SH, Wang KS (2014a) Streptomyces panaciradicis sp. nov., a β-glucosidase-producing bacterium isolated from rhizoplane of ginseng. Int J Syst Evol Microbiol 64:3816–3820. https://doi.org/10.1099/ijs.0.061705-0
Lee S, Lee YH, Park JM, Bai DH, Jang JK, Park YS (2014b) Bioconversion of ginsenosides from red ginseng extract using Candida allociferrii JNO301 isolated from Meju. Mycobiology 31:368–375. https://doi.org/10.5941/MYCO.2014.42.4.368
Li Y, Long QL, Ding WL, Zhao DY (2014) Mitigative effect of micribial degradation on autotoxicity of Panax ginseng. China J Chin Mater Med 39:2868. https://doi.org/10.4268/cjcmm20141515
Li YL, Wang BY, Chang YF, Xu YB, Huang XQ, Zhang JB, Cai ZC, Zhao J (2018) Effects of reductive soil disinfestation on obstacles and growth of replant seedlings in Sanqi ginseng mono-cropped soils. Acta Pedol Sin. https://doi.org/10.11766/trxb201806110164
Liu LL, Chen SH, Zhao J, Zhou X, Wang BY, Li YL, Zheng GQ, Zhang JB, Cai ZC, Huang XQ (2018) Watermelon planting is capable to restructure the soil microbiome that regulated by reductive soil disinfestation. Appl Soil Ecol 129:52–60. https://doi.org/10.1016/j.apsoil.2018.05.004
Lu RK (2000) Soil agricultural chemical analysis method. China Agricultural Science and Technology Press, Beijing
Mazzola M (2004) Assessment and management of soil microbial community structure for disease suppression. Annu Rev Phytopathol 42:35–59
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. https://doi.org/10.1038/ismej.2011.139
Meiners SJ, Phipps KK, Pendergast TH, Canam T, Carson WP (2017) Soil microbial communities alter leaf chemistry and influence allelopathic potential among coexisting plant species. Oecologia 183:1155–1165. https://doi.org/10.1007/s00442-017-3833-4
Molendijk LPG, Bleeker PO, Lamers JG, Runia WT (2009) Perspectives of anaerobic soil disinfestation. Acta Hortic 883:277–283. https://doi.org/10.17660/ActaHortic.2010.883.34
Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A (2013) Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 97:3801–3809. https://doi.org/10.1007/s00253-013-4826-9
Ng T (2006) Pharmacological activity of sanchi ginseng (Panax notoginseng). J Pharm Pharmacol 58:1007–1019. https://doi.org/10.1211/jpp.58.8.0001
Nicol RW, Traquair JA, Bernards MA (2002) Ginsenosides as host resistance factors in American ginseng (Panax quinquefolius). Can J Bot 80:557–562. https://doi.org/10.1139/b02-034
Nicol RW, Yousef L, Traquair JA, Bernards MA (2003) Ginsenosides stimulate the growth of soilborne pathogens of American ginseng. Phytochemistry 64:257–264. https://doi.org/10.1016/s0031-9422(03)00271-1
Niro E, Marzaioli R, Crescenzo SD, D’Abrosca B, Castaldi S, Esposito A, Fiorentino A, Rutigliano FA (2016) Effects of the allelochemical coumarin on plants and soil microbial community. Soil Biol Biochem 95:30–39. https://doi.org/10.1016/j.soilbio.2015.11.028
Peters RD, Sturz AV, Carter MR, Sanderson JB (2003) Developing disease-suppressive soils through crop rotation and tillage management practices. Soil Tillage Res 72:181–192. https://doi.org/10.1016/S0167-1987(03)00087-4
Ren X, Yan ZQ, He XF, Li XZ, Qin B (2017) Allelochemicals from rhizosphere soils of Glycyrrhiza uralensis Fisch: discovery of the autotoxic compounds of a traditional herbal medicine. Ind Crop Prod 97:302–307. https://doi.org/10.1016/j.indcrop.2016.12.035
Shen H, Leung WI, Ruan JQ, Li SL, Lei PC, Wang YT, Yan R (2013) Biotransformation of ginsenoside Rb1 via the gypenoside pathway by human gut bacteria. Chin Med 8:22. https://doi.org/10.1186/1749-8546-8-22
Tan Y, Cui YS, Li HY, Kuang AX, Li XR, Wei YL, Ji XL (2017) Diversity and composition of rhizospheric soil and root endogenous bacteria in Panax notoginseng during continuous cropping practices. J Basic Microbiol 57:337–344. https://doi.org/10.1002/jobm.201600464
Ueki A, Kaku N, Ueki K (2018) Role of anaerobic bacteria in biological soil disinfestation for elimination of soil-borne plant pathogens in agriculture. Appl Microbiol Biotechnol 102:6309–6318. https://doi.org/10.1007/s00253-018-9119-x
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wen T, Huang XQ, Zhang JB, Cai ZC (2016) Effects of biological soil disinfestation and water regime on suppressing Artemisia selengensis root rot pathogens. J Soils Sediments 16:215–225. https://doi.org/10.1007/s11368-015-1172-9
Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12:259–276. https://doi.org/10.1016/S0958-1669(00)00209-3
Wu LJ, Zhao YH, Guan YM, Pang SF (2008) A review on studies of the reason and control methods of succession cropping obstacle of Panax ginseng C.A.Mey. Spec Wild Econ Anim. Plant Res 2:68–72. https://doi.org/10.3969/j.issn.1001-4721.2008.02.021
Xie M, Yan ZQ, Ren X, Li XZ, Qin B (2017) Codonopilate A, a triterpenyl ester as main autotoxin in cultivated soil of Codonopsis pilosula (Franch.) Nannf. J Agric Food Chem 65:2032–2038. https://doi.org/10.1021/acs.jafc.6b04320
Xiong W, Zhao QY, Zhao J, Xun WB, Li R, Zhang RF, Wu HS, Shen QR (2015) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microb Ecol 70:209–218. https://doi.org/10.1007/s00248-014-0516-0
Yang M, Zhang Y, Qi L, Mei XY, Liao JJ, Ding XP, Deng WP, Fan LM, He XH, Vivanco JM, Li CY, Zhu YY, Zhu SS (2014) Plant-plant-microbe mechanisms involved in soil-borne disease suppression on a maize and pepper intercropping system. PLoS One 9:e115052. https://doi.org/10.1371/journal.pone.0115052
Yang M, Zhang XD, Xu YG, Mei XY, Jiang BB, Liao JJ, Yin ZB, Zheng JF, Zhao Z, Fan LM, He XH, Zhu YY, Zhu SS (2015) Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 10:e0118555. https://doi.org/10.1371/journal.pone.0118555
Zhang ZY, Lin WX (2009) Continuous cropping obstacle and allelopathic autotoxicity of medicinal plants. Chi J Eco-Agric 17:189–196. https://doi.org/10.3724/SP.J.1011.2009.00189
Zhang SS, Shi FQ, Yang WZ, Xiang ZY, Kang HM, Duan ZL (2015) Autotoxicity as a cause for natural regeneration failure in Nyssa yunnanensis and its implications for conservation. Isr J Plant Sci 62:187–197. https://doi.org/10.1080/07929978.2015.1064630
Zhang W, Wang HW, Wang XX, Xie XG, Siddikee MA, Xu RS, Dai CC (2016) Enhanced nodulation of peanut when co-inoculated with fungal endophyte Phomopsis liquidambari and Bardyrhizobium. Plant Physiol Biochem 98:1–11. https://doi.org/10.1016/j.plaphy.2015.11.002
Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen QR, Zhang RF (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. PLoS One 9:e85301. https://doi.org/10.1371/journal.pone.0085301
Zhao J, Li YL, Wang BY, Huang XQ, Yang L, Lan T, Zhang JB, Cai ZC (2017) Comparative soil microbial communities and activities in adjacent Sanqi ginseng monoculture and maize-Sanqi ginseng systems. Appl Soil Ecol 120:89–96. https://doi.org/10.1016/j.apsoil.2017.08.002
Zhao J, Zhou X, Jiang AQ, Fan JZ, Lan T, Zhang JB, Cai ZC (2018) Distinct impacts of reductive soil disinfestation and chemical soil disinfestation on soil fungal communities and memberships. Appl Microbiol Biotechnol 102:7623–7634. https://doi.org/10.1007/s00253-018-9107-1
Zhou X, Yu G, Wu F (2012) Soil phenolics in a continuously monocropped cucumber (Cucumis sativus L.) system and their effects on cucumber seedling growth and soil microbial communities. Eur J Soil Sci 63:332–340. https://doi.org/10.1111/j.1365-2389.2012.01442.x
Zhu TB, Zhang JB, Yang WY, Cai ZC (2013) Effects of organic material amendment and water content on NO, N2O, and N2 emissions in a nitrate-rich vegetable soil. Biol Fertil Soils 49:153–163. https://doi.org/10.1007/s00374-012-0711-4
Acknowledgements
We would like to thank the staffs in Miaoxiang Sanqi Technology Co., Ltd. for managing the field experiment and collecting the growth data of replant seedlings.
Funding
This study was financially supported by the National Natural Science Foundation of China (41701277, 41771281), the National Key Research and Development Program of China (2017YFD0200600), the China Postdoctoral Science Foundation (2018 M630573), the Startup Funds of Nanjing Normal University (184080H202B136), the Postgraduate Research & Practice Innovation Program of Jiangsu Province, China (KYCX18_1201), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, and the Key Subjects of Jiangsu Province (Ecology).
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Li, Y., Wang, B., Chang, Y. et al. Reductive soil disinfestation effectively alleviates the replant failure of Sanqi ginseng through allelochemical degradation and pathogen suppression. Appl Microbiol Biotechnol 103, 3581–3595 (2019). https://doi.org/10.1007/s00253-019-09676-4
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DOI: https://doi.org/10.1007/s00253-019-09676-4