Skip to main content
SpringerLink
Log in

Identification of phytotoxic metabolites released from Rehmannia glutinosa suggest their importance in the formation of its replant problem

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

The yield and quality of medicinal tubers of Rehmannia glutinosa are seriously restricted by replanting problems. However, the origin and identification of the potential allelochemicals associated with this issue have not been well described. Therefore, in a series of related studies, we aimed to identify the key phytotoxic metabolites released from R. glutinosa.

Methods

R. glutinosa residues were harvested and extracted for metabolic profiling and bioassay-directed identification. Metabolites in the leaf, tuber, and soil surrounding R. glutinosa roots were profiled using high pressure liquid chromatography coupled to a quadrupole/time of flight mass spectormeter. A Petri dish-filter paper and modified Parker bioassay were used to evaluate the phytotoxicity of plant residues and candidate allelochemicals.

Results

Seventeen metabolites specific to R. glutinosa were identified/annotated using non-targeted metabolic profiling combined with known standards. Assay results suggested an iridoid glycoside and several phenylethanoid glycosides as key allelochemicals originating from R. glutinosa.

Conclusion

Identification of bioactive metabolites in planta and in the rhizosphere has increased our understanding of the phytochemistry of R. glutinosa. Further evaluation of the soil persistence and ecological functions of these bioactive compounds will be important for determination of the specific mechanisms associated with R. glutinosa replanting issues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

UHPLC QTOF MS:

high pressure liquid chromatography coupled to quadrupole/time of flight mass spectrometry

MPP:

Agilent Mass Profiler Professional 13.0

TCC:

Total compound chromatogram

EIC:

Extracted ion chromatogram

L:

R. glutinosa leaf.

T:

R. glutinosa tuber.

R:

R. glutinosa rhizosphere soil.

References

  • Abdelmigid HM, Morsi MM (2017) Cytotoxic and molecular impacts of allelopathic effects of leaf residues of Eucalyptus globulus on soybean (Glycine max). J Genet Eng Biotechnol 15:297–302. https://doi.org/10.1016/j.jgeb.2017.08.005

    Article  PubMed  PubMed Central  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159

    Article  CAS  Google Scholar 

  • Barber D, Martin J (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80

    Article  CAS  Google Scholar 

  • Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83. https://doi.org/10.1023/A:1026290508166

    Article  CAS  Google Scholar 

  • Bhowmik PC, Inderjit (2003) Challenges and opportunities in implementing allelopathy for natural weed management. Crop Prot 22:661–671. https://doi.org/10.1016/S0261-2194(02)00242-9

    Article  Google Scholar 

  • Blum U (1998) Effects of microbial utilization of phenolic acids and their phenolic acid breakdown products on Allelopathic interactions. J Chem Ecol 24:685–708

    Article  CAS  Google Scholar 

  • Bowers JHW, R.R. (2007) The nature and properties of soils, 14 edition. Prentice hall

  • Chase MW et al (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Chen HH, H.R; Xiong, J; Qi, X. H; Zhang, C. Y; Lin, W. X (2007) Effects of successive cropping Rehmannia glutinosa on rhizosphere soil microbial flora an enzyme activities. J Appl Ecol 18:2755–2759

  • Chen BJW, During HJ, Anten NPR (2012) Detect thy neighbor: identity recognition at the root level in plants. Plant Sci 195:157–167

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Gu L, Li M, Xu N, Feng F, Liu G, Zhang B, Gong D, Zhang J, Liu H, Zhang Z (2018) Identification of Rehmannia glutinosa L. NB-ARC family proteins and their typical changes under consecutive monoculture stress. Acta Physiol Plant 40:95

    Article  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. https://doi.org/10.1023/A:1020809400075

    Article  CAS  Google Scholar 

  • Du J, Yin W, Li J, Zhang Z (2009) Dynamic change of phenolic acids in soils around rhizosphere of replanted Rehmannia glutinosa China. Journal of Chinese Materia Medica 34:948–952

    Google Scholar 

  • Hartung AC, Stephens CT (1983) Effects of allelopathic substances produced by asparagus on incidence and severity of asparagus decline due to Fusarium crown rot. J Chem Ecol 9:1163–1174

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Qin T, Huang Y, Liu Z, Bo R, Hu Y, Liu J, Wu Y, Wang D (2016) Rehmannia glutinosa polysaccharide liposome as a novel strategy for stimulating an efficient immune response and their effects on dendritic cells. Int J Nanomedicine 11:6795–6808. https://doi.org/10.2147/IJN.S119108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hung PV, Hatcher DW, Barker W (2011) Phenolic acid composition of sprouted wheats by ultra-performance liquid chromatography (UPLC) and their antioxidant activities. Food Chem 126:1896–1901

    Article  CAS  PubMed  Google Scholar 

  • Inderjit, Weston LA, Duke SO (2005) Challenges, achievements and opportunities in allelopathy research. J Plant Interact 1:69–81

    Article  CAS  Google Scholar 

  • Ismail LD, El-Azizi MM, Khalifa TI, Stermitz FR (1995) Verbascoside derivatives and iridoid glycosides from Penstemon crandallii. Phytochemistry 39:1391–1393

    Article  CAS  PubMed  Google Scholar 

  • Jiménez C, Riguera R (1994) Phenylethanoid glycosides in plants: structure and biological activity. Nat Prod Rep 11:591–606

    Article  PubMed  Google Scholar 

  • Kong CH, Li HB, Hu F, Xu XH, Wang P (2006) Allelochemicals released by rice roots and residues in soil. Plant Soil 288:47–56. https://doi.org/10.1007/s11104-006-9033-3

    Article  CAS  Google Scholar 

  • Kong CH, Zhang SZ, Li YH, Xia ZC, Yang XF, Meiners SJ, Wang P (2018) Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals. Nat Commun 9:3867. https://doi.org/10.1038/s41467-018-06429-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruidhof HM, Bastiaans L, Kropff MJ (2009) Cover crop residue management for optimizing weed control. Plant Soil 318:169–184. https://doi.org/10.1007/s11104-008-9827-6

    Article  CAS  Google Scholar 

  • Lee B, Shim I, Lee H, Hahm DH (2011) Rehmannia glutinosa ameliorates scopolamine-induced learning and memory impairment in rats. J Microbiol Biotechnol 21:874–883

    Article  PubMed  Google Scholar 

  • Li ZF, Yang YQ, Xie DF, Zhu LF, Zhang ZG, Lin WX (2012) Identification of autotoxic compounds in fibrous roots of Rehmannia (Rehmannia glutinosa Libosch.). PLoS One 7:e28806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Yang Y, Li X, Gu L, Wang F, Feng F, Tian Y, Wang F, Wang X, Lin W, Chen X, Zhang Z (2015) Analysis of integrated multiple ‘omics’ datasets reveals the mechanisms of initiation and determination in the formation of tuberous roots in Rehmannia glutinosa. J Exp Bot 66:5837–5851

    Article  CAS  PubMed  Google Scholar 

  • Li ZF, He CL, Wang Y, Li MJ, Dai YJ, Wang T, Lin W (2016) Enhancement of trichothecene mycotoxins of Fusarium oxysporum by ferulic acid aggravates oxidative damage in Rehmannia glutinosa Libosch. Sci Rep 6:33962. https://doi.org/10.1038/srep33962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Yang Y, Feng F, Zhang B, Chen S, Yang C, Gu L, Wang F, Zhang J, Chen A, Lin W, Chen X, Zhang Z (2017) Differential proteomic analysis of replanted Rehmannia glutinosa roots by iTRAQ reveals molecular mechanisms for formation of replant disease. BMC Plant Biol 17:116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lou Y, Davis AS, Yannarell AC (2016) Interactions between allelochemicals and the microbial community affect weed suppression following cover crop residue incorporation into soil. Plant Soil 399:357–371. https://doi.org/10.1007/s11104-015-2698-8

    Article  CAS  Google Scholar 

  • Machinet GE, Bertrand I, Barriere Y, Chabbert B, Recous S (2011) Impact of plant cell wall network on biodegradation in soil: role of lignin composition and phenolic acids in roots from 16 maize genotypes. Soil Biol Biochem 43:1544–1552. https://doi.org/10.1016/j.soilbio.2011.04.002

    Article  CAS  Google Scholar 

  • Mccully ME, Miller C, Sprague SJ, Huang CX, Kirkegaard JA (2008) Distribution of glucosinolates and Sulphur-rich cells in roots of field-grown canola (Brassica napus). New Phytol 180:193–205

    Article  CAS  PubMed  Google Scholar 

  • Molisch H (1937) Der Einfluss einer Pflanze auf die andere. Allelopathie Fischer Jena

  • Narula N, Kothe E, Behl RK (2009) Role of root exudates in plant-microbe interactions. J Appl Bot Food Qual 82:122–130

    CAS  Google Scholar 

  • Park SU, Il Park N, Kim YK, Suh SY, Eom SH, Lee SY (2009) Application of plant biotechnology in the medicinal plant, Rehmannia glutinosa Liboschitz. J Med Plant Res 3:1258–1263

    CAS  Google Scholar 

  • Parker C (1966) The importance of shoot entry in the action of herbicides applied to the soil. Weeds 14:117–121

    Article  CAS  Google Scholar 

  • Qi M, Xiong AZ, Li PF, Yang QM, Yang L, Wang ZT (2013) Identification of acteoside and its major metabolites in rat urine by ultra-performance liquid chromatography combined with electrospray ionization quadrupole time-of-flight tandem mass spectrometry. J Chromatogr B 940:77–85. https://doi.org/10.1016/j.jchromb.2013.09.023

    Article  CAS  Google Scholar 

  • Rasmann S, Turlings TC (2016) Root signals that mediate mutualistic interactions in the rhizosphere. Curr Opin Plant Biol 32:62–68

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for Iron Phytosiderophores in roots of grasses. Plant Physiol 80:175–180

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan P, Delhaize E, Jones D (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  CAS  PubMed  Google Scholar 

  • Skoneczny D, Weston P, Zhu X, Gurr G, Callaway R, Weston L (2015) Metabolic profiling of pyrrolizidine alkaloids in foliage of two Echium spp. invaders in Australia—a case of novel weapons? Int J Mol Sci 16:26721–26737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skoneczny D, Weston PA, Zhu X, Gurr GM, Callaway RM, Barrow RA, Weston LA (2017) Metabolic profiling and identification of Shikonins in root periderm of two invasive Echium spp. weeds in Australia. Molecules 22. https://doi.org/10.3390/molecules22020330

  • Steehler JK (2007) Introduction to mass spectrometry: instrumentation, applications, and strategies for data interpretation, 4th edition (by J. Throck Watson and O. David Sparkman). Journal of chemical education 86:págs. In: 810–810

    Google Scholar 

  • Stringlis IA, Yu K, Feussner K, de Jonge R, van Bentum S, van Verk MC, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci U S A 115:E5213–E5222. https://doi.org/10.1073/pnas.1722335115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uren N (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown. Plants English:1–21

  • van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265

    Article  CAS  PubMed  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JM, Pei LX, Zhang YY, Cheng YX, Niu CL, Cui Y, Feng WS, Wang GF (2018a) Ethanol extract of Rehmannia glutinosa exerts antidepressant-like effects on a rat chronic unpredictable mild stress model by involving monoamines and BDNF. Metab Brain Dis 33:885–892. https://doi.org/10.1007/s11011-018-0202-x

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Kwak M, Lee PC, Jin JO (2018b) Rehmannia glutinosa polysaccharide promoted activation of human dendritic cells. Int J Biol Macromol 116:232–238. https://doi.org/10.1016/j.ijbiomac.2018.04.144

    Article  CAS  PubMed  Google Scholar 

  • Weston LA, Duke SO (2003) Weed and crop allelopathy. Crit Rev Plant Sci 22:367–389

    Article  CAS  Google Scholar 

  • Weston LA, Harmon R, Mueller S (1989) Allelopathic potential of sorghum-sudangrass hybrid (sudex). J Chem Ecol 15:1855–1865

    Article  CAS  PubMed  Google Scholar 

  • Weston LA, Ryan PR, Watt M (2012) Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. J Exp Bot 63:3445–3454

    Article  CAS  PubMed  Google Scholar 

  • Wink M (2010) Annual plant reviews volume 39: functions and biotechnology of plant secondary metabolites, Second edition

  • Wu Z, Wang M, Liu X, Chen H, Jia X (2009) Phenolic compounds accumulation in continuously cropped Rehmannia glutinosa soil and their effects on R. glutinosa growth. Chin J Eco 28:660–664

    Google Scholar 

  • Wu PS, Wu SJ, Tsai YH, Lin YH, Chao JC (2011) Hot water extracted Lycium barbarum and Rehmannia glutinosa inhibit liver inflammation and fibrosis in rats. Am J Chin Med 39:1173–1191. https://doi.org/10.1142/S0192415X11009482

    Article  PubMed  Google Scholar 

  • Wu LK, Li ZF, Li J, Khan MA, Huang WM, Zhang ZY, Lin WX (2013) Assessment of shifts in microbial community structure and catabolic diversity in response to Rehmannia glutinosa monoculture. Appl Soil Ecol 67:1–9. https://doi.org/10.1016/j.apsoil.2013.02.008

    Article  Google Scholar 

  • Wu L, Wang J, Huang W, Wu H, Chen J, Yang Y, Zhang Z, Lin W (2016a) Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture. Sci Rep 6:19101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu LK, Wu HM, Chen J, Wang JY, Lin WX (2016b) Microbial community structure and its temporal changes in Rehmannia glutinosa rhizospheric soils monocultured for different years. Eur J Soil Biol 72:1–5. https://doi.org/10.1016/j.ejsobi.2015.12.002

    Article  Google Scholar 

  • Wu L, Chen J, Xiao Z, Zhu X, Wang J, Wu H, Wu Y, Zhang Z, Lin W (2018a) Barcoded pyrosequencing reveals a shift in the bacterial community in the rhizosphere and rhizoplane of Rehmannia glutinosa under consecutive monoculture. Int J Mol Sci 19:850

    Article  CAS  PubMed Central  Google Scholar 

  • Wu LK, Chen J, Khan MU, Wang J, Wu H, Xiao Z, Zhang Z, Lin W (2018b) Rhizosphere fungal community dynamics associated with Rehmannia glutinosa replant disease in a consecutive monoculture regime. Phytopathology 108:1493–1500. https://doi.org/10.1094/Phyto-02-18-0038-R

    Article  PubMed  Google Scholar 

  • Wu LK, Wang J, Wu H, Chen J, Xiao Z, Qin X, Zhang Z, Lin W (2018c) Comparative metagenomic analysis of rhizosphere microbial community composition and functional potentials under Rehmannia glutinosa consecutive monoculture. Int J Mol Sci 19:2394. https://doi.org/10.3390/ijms19082394

    Article  CAS  PubMed Central  Google Scholar 

  • Xue Z, Yang B (2016) Phenylethanoid glycosides: research advances in their phytochemistry, pharmacological activity and pharmacokinetics. Molecules 21:991

    Article  CAS  PubMed Central  Google Scholar 

  • Xue B, Ma B, Zhang Q, Li X, Zhu J, Liu M, Wu X, Wang C, Wu Z (2015) Pharmacokinetics and tissue distribution of Aucubin, Ajugol and Catalpol in rats using a validated simultaneous LC–ESI-MS/MS assay. J Chromatogr B 1002:245–253

    Article  CAS  Google Scholar 

  • Yang YH, Li MJ, Chen XJ, Wang PF, Wang FQ, Lin WX, Yi YJ, Zhang ZW, Zhang ZY (2014) De novo characterization of the Rehmannia glutinosa leaf transcriptome and analysis of gene expression associated with replanting disease. Mol Breed 34:905–915

    Article  CAS  Google Scholar 

  • Yang M, Zhang X, Xu Y, Mei X, Jiang B, Liao J, Yin Z, Zheng J, Zhao Z, Fan L, He X, Zhu Y, Zhu S (2015a) Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 10:e0118555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang YH, Li MJ, Li XY, Chen XJ, Lin WX, Zhang ZY (2015b) Transcriptome-wide identification of the genes responding to replanting disease in Rehmannia glutinosa L. roots. Mol Biol Rep 42:881–892. https://doi.org/10.1007/s11033-014-3825-y

    Article  CAS  PubMed  Google Scholar 

  • Ye S, Yu J, Peng Y, Zheng J, Zou L (2004) Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263:143–150

    Article  CAS  Google Scholar 

  • Young C, Chou T (1985) Autointoxication in residues of Asparagus officinalis L. Plant Soil 85:385–393

    Article  Google Scholar 

  • Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139. https://doi.org/10.1016/S0305-1978(02)00150-3

    Article  CAS  Google Scholar 

  • Zhang S, Gao Z (2000) Continuous cropping obstacle and rhizospheric microecology. II. Root exudates and phenolic acids. J Appl Ecol 11:152–156

    CAS  Google Scholar 

  • Zhang Z, Lin W (2009) Continuous cropping obstacle and allelopathic autotoxicity of medicinal plants. Chin J Eco-Agric 17:189–196

    Article  CAS  Google Scholar 

  • Zhang R, Zhou J, Jia Z, Zhang Y, Gu G (2004) Hypoglycemic effect of Rehmannia glutinosa oligosaccharide in hyperglycemic and alloxan-induced diabetic rats and its mechanism. J Ethnopharmacol 90:39–43

    Article  CAS  PubMed  Google Scholar 

  • Zhang RX, Li MX, Jia ZP (2008) Rehmannia glutinosa: review of botany, chemistry and pharmacology. J Ethnopharmacol 117:199–214. https://doi.org/10.1016/j.jep.2008.02.018

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Li XZ, Feng FJ, Gu L, Zhang JY, Zhang LJ, Zhang ZY (2015) Correlation of allelopathy of Rehmannia glutinosa root exudates and their phenolic acids contents. Chin Med Mat 38:659

    CAS  Google Scholar 

  • Zhang B, Li X, Wang F, Li M, Zhang J, Gu L, Zhang L, Tu W, Zhang Z (2016) Assaying the potential autotoxins and microbial community associated with Rehmannia glutinosa replant problems based on its 'autotoxic circle'. Plant Soil 407:307–322. https://doi.org/10.1007/s11104-016-2885-2

    Article  CAS  Google Scholar 

  • Zhou F, Zhao Y, Li M, Xu T, Zhang L, Lu B, Wu X, Ge Z (2017) Degradation of phenylethanoid glycosides in Osmanthus fragrans Lour. Flowers and its effect on anti-hypoxia activity. Sci Rep 7:10068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Skoneczny D, Weidenhamer JD, Mwendwa JM, Weston PA, Gurr GM, Callaway RM, Weston LA (2016) Identification and localization of bioactive naphthoquinones in the roots and rhizosphere of Paterson’s curse (Echium plantagineum), a noxious invader. J Exp Bot 67:3777–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We acknowledge the contribution of Russell Barrow in reviewing the paper and providing helpful suggestions, and the help of Xiaocheng Zhu, Saliya Gurusinghe and Graeme Heath from Graham Centre for Agricultural Innovation, Charles Sturt University. This research was supported by the Scientific Research Foundation of Graduate School of Fujian Agriculture and Forestry University under grant 324-1122yb028, the National Science Foundation of China (Grant no. 81603243), the National Key R&D Program of China (2017YFC1700705) and the Natural Science Foundation of Fujian Province of China (No.2017 J01804).

Author information

Authors and Affiliations

  1. Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou, 350002, People’s Republic of China

    Bao Zhang, Li Gu, Mingjie Li, Jianming Wang & Zhongyi Zhang

  2. Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, NSW, 2650, Australia

    Paul A. Weston & Leslie A. Weston

  3. Henan Provincial People’s Hospital, Zhengzhou, 450003, People’s Republic of China

    Bingyong Zhang

  4. College of Agronomy, Henan Agricultural University, Zhengzhou, 450002, People’s Republic of China

    Fengqing Wang

  5. Henan Province Chinese Medicine Research Institute, Zhengzhou, 450004, People’s Republic of China

    Wanqian Tu

Authors
  1. Bao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul A. Weston
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bingyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mingjie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fengqing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wanqian Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jianming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Leslie A. Weston
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhongyi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongyi Zhang.

Additional information

Responsible Editor: Matthew G. Bakker.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 6953 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, B., Weston, P.A., Gu, L. et al. Identification of phytotoxic metabolites released from Rehmannia glutinosa suggest their importance in the formation of its replant problem. Plant Soil 441, 439–454 (2019). https://doi.org/10.1007/s11104-019-04136-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04136-4

Keywords

Search

Navigation