Atractylodes lancea volatiles induce physiological responses in neighboring peanut plant during intercropping

Abstract

Aims

Plant volatiles serve as airborne semiochemicals, bridging the interactions between the plant and environment. Intercropping of a Chinese medicinal herb, Atractylodes lancea, with peanut plants greatly improves peanut growth, leading to a reduction of soil-borne disease. The underlying mechanism of peanut responding to the intercropped A. lancea is unknown. We here explored the response of the above- and belowground peanut parts to volatiles produced by the aboveground parts of A. lancea.

Methods

Closed cultivation system was used. Composition of volatiles released by A. lancea plant was first determined using headspace solid phase microextraction–gas chromatography/mass spectrometry (SPME-GC-MS). Then, physiological responses of peanut were explored via enzymes activity assay and root secretions. Changes in the peanut rhizosphere fungal and bacterial communities were analyzed by Illumina sequencing.

Results

The intercropped A. lancea volatiles induced a physiological response in peanut, which includes the increased catalase and phenylalanine ammonia lyase activity in peanut leaf, and improvement of peanut growth. Secretion of organic acids by the peanut root was increased in response to volatile treatment. Pyrosequencing of the whole internal transcribed spacer and 16S rRNA amplicons revealed significant differences in microbial diversity and composition in peanut rhizosphere upon volatile treatment.

Conclusions

In the intercropping, A. lancea volatiles play a key role in influencing the growth of a neighbouring peanut plant, e.g., increasing biomass and affecting root colonization by soil microorganisms, which may increase plant protection against pathogens. Intercropping patterns could be designed accordingly to increase crop performance.

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  1. Aggarwal A, Ezaki B, Tripathi BN (2015) Two detoxification mechanisms by external malate detoxification and anti-peroxidation enzymes cooperatively confer aluminium tolerance in the roots of wheat (Triticum aestivum L.). Environ Exp Bot 120:43–54

    CAS  Google Scholar 

  2. Ahmed S, Zhan C, Yang Y, Wang X, Yang T, Zhao Z, Hu X (2016) The transcript profile of a traditional Chinese medicine, Atractylodes lancea, revealing its sesquiterpenoid biosynthesis of the major active components. PloS One 11(3):e0151975

    PubMed  PubMed Central  Google Scholar 

  3. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98

    CAS  PubMed  Google Scholar 

  4. Baldwin IT (2010) Plant volatiles. Curr Biol 20(9):392–397

    Google Scholar 

  5. Baldwin IT, Halitschke R, Paschold A, Von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “talking trees” in the genomics era. Science 311:812–815

    CAS  PubMed  Google Scholar 

  6. Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201

    CAS  PubMed  Google Scholar 

  7. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256(1):67–83

    CAS  Google Scholar 

  9. Boudreau MA (2013) Disease in intercropping systems. Annu Rev Phytopathol 51:499–519

    CAS  PubMed  Google Scholar 

  10. Boudreau MA, Shew BB, Duffie Andrako LE (2015) Impact of intercropping on epidemics of groundnut leaf spots: defining constraints and opportunities through a 7-year field study. Plant Pathol 65:601–611

    Google Scholar 

  11. Bowler C, van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Ann Rev Plant Physiol 43:83–116

    CAS  Google Scholar 

  12. Brooker RW, Karley AJ, Newton AC, Pakeman RJ, Schöb C (2016) Facilitation and sustainable agriculture: a mechanistic approach to reconciling crop production and conservation. Funct Ecol 30:98–107

    Google Scholar 

  13. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. P Natl Acad Sci USA 108:4516–4522

    CAS  Google Scholar 

  14. Carvalho FP (2017) Pesticides, environment, and food safety. Food Energy Secur 6(2):48–60

    Google Scholar 

  15. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Dai CC, Xie H, Wang XX, Li PD, Zhang TL, Li YL, Tan X (2009) Intercropping peanut with traditional Chinese medicinal plants improves soil microcosm environment and peanut production in subtropical China. Afr J Biotechnol 8:3739–3746

    CAS  Google Scholar 

  17. Dai CC, Chen Y, Wang XX, Li PD (2013) Effects of intercropping of peanut with the medicinal plant Atractylodes lancea on soil microecology and peanut yield in subtropical China. Agroforest Syst 87:416–427

    Google Scholar 

  18. de Vos M, Jander G (2010) Volatile communication in plant–aphid interactions. Curr Opin Plant Biol 13(4):366–371

    PubMed  Google Scholar 

  19. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72(3):313–327

    CAS  PubMed  Google Scholar 

  20. Duragannavar FM, Patil BN, Halikatti SI, Palled YB, Patil PL, Mohankumar HD (2013) Yield, nutrient uptake and economics as influenced by chilli + cotton intercropping system. Karnataka J Agri Sci 26(1):20–25

    Google Scholar 

  21. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    CAS  PubMed  Google Scholar 

  22. Evtushenko LI, Takeuchi M (2006) The family microbacteriaceae. In: M Dworkin, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (ed) The Prokaryotes, 3rd edn, Springer, New York, pp 1020–1098

  23. FAO (1998) FAO, ISRIC, ISSS World reference base for soil resources. World Soil Resources Reports 84. Rome, Italy

    Google Scholar 

  24. Goel R, Kumar V, Suyal DK, Dash B, Kumar P, Soni R (2017) Root-associated bacteria: rhizoplane and endosphere. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 161–176

    Google Scholar 

  25. Guo FQ, Huang LF, Zhou SY, Zhang TM, Liang YZ (2006) Comparison of the volatile compounds of Atractylodes medicinal plants by headspace solid-phase microextraction-gas chromatography–mass spectrometry. Anal Chim Acta 570(1):73–78

    CAS  Google Scholar 

  26. Guo M, Feng J, Zhang P, Jia L, Chen K (2015) Postharvest treatment with trans-2-hexenal induced resistance against Botrytis cinerea in tomato fruit. Australas Plant Path 44(1):121–128

    CAS  Google Scholar 

  27. Hauggaard-Nielsen H, Gooding M, Ambus P, Corre-Hellou G, Crozat Y, Dahlmann C, Jensen ES (2009) Pea–barley intercropping for efficient symbiotic N2-fixation, soil N acquisition and use of other nutrients in European organic cropping systems. Field Crop Res 113(1):64–71

    Google Scholar 

  28. Heil M, Bueno JCS (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104(13):5467–5472

    CAS  PubMed  Google Scholar 

  29. Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25(3):137–144

    PubMed  Google Scholar 

  30. Horrigan L, Lawrence RS, Walker P (2002) How sustainable agriculture can address the environmental and human health harms of industrial agriculture. Environ Health Persp 110(5):445–456

    Google Scholar 

  31. Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B et al (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:1–13

    Google Scholar 

  32. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M, Douglas B (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22(21):5271–5277

    PubMed  Google Scholar 

  33. Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse US (2010) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytol 185(2):577–588

    CAS  PubMed  Google Scholar 

  34. Latati M, Blavet D, Alkama N, Laoufi H, Drevon JJ, Gerard F, Ounane SM (2014) The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 385(1–2):181–191

    CAS  Google Scholar 

  35. Le Cointe R, Simon TE, Delarue P, Hervé M, Leclerc M, Poggi S (2016) Reducing the use of pesticides with site-specific application: the chemical control of Rhizoctonia solani as a case of study for the management of soil-borne diseases. PLoS One 11:e0163221

    PubMed  PubMed Central  Google Scholar 

  36. Lewin GR, Carlos C, Chevrette MG, Horn HA, McDonald BR, Stankey RJ, Currie CR (2016) Evolution and ecology of Actinobacteria and their bioenergy applications. Annu Rev Microbiol 70:235–254

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Li XG, Zhang TL, Wang XX, Hua K, Zhao L, Han ZM (2013) The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci 9(2):164–173

    PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  39. Li XG, Wang XX, Dai CC, Zhang TL, Xie XG, Ding CF, Wang HW (2014b) Effects of intercropping with Atractylodes lancea and application of bio-organic fertiliser on soil invertebrates, disease control and peanut productivity in continuous peanut cropping field in subtropical China. Agroforest Syst 88:41–52

    Google Scholar 

  40. Li XG, Boer WD, Zhang YN, Ding CF, Zhang TL, Wang XX (2018) Suppression of soil-borne Fusarium pathogens of peanut by intercropping with the medicinal herb Atractylodes lancea. Soil Biol Biochem 116:120–130

    CAS  Google Scholar 

  41. Loreto F, Dicke M, Schnitzler JP, Turlings TC (2014) Plant volatiles and the environment. Plant Cell Environ 37(8):1905–1908

    PubMed  Google Scholar 

  42. Lu SW, Kroken S, Lee BN, Robbertse B, Churchill AC, Yoder OC, Turgeon BG (2003) A novel class of gene controlling virulence in plant pathogenic ascomycete fungi. Proc Natl Acad Sci USA 100(10):5980–5985

    CAS  PubMed  Google Scholar 

  43. Lu L, Yin S, Liu X, Zhang W, Gu T, Shen Q, Qiu H (2013) Fungal networks in yield-invigorating and-debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194

    CAS  Google Scholar 

  44. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Toth I (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13(6):614–629

    PubMed  PubMed Central  Google Scholar 

  45. Masuda Y, Kadokura T, Ishii M, Takada K, Kitajima J (2015) Hinesol, a compound isolated from the essential oils of Atractylodes lancea rhizome, inhibits cell growth and induces apoptosis in human leukemia HL-60 cells. J Nat Med 69:332–339

    CAS  PubMed  Google Scholar 

  46. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17(5):303–310

    Google Scholar 

  47. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van Der Voort M, Schneider JHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332(6033):1097–1100

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Mhedbihajri N, Jacques MA, Koebnik R (2011) Adhesion mechanisms of plant-pathogenic Xanthomonadaceae. Adv Exp Med Biol 715:71–89

    CAS  Google Scholar 

  49. Mishra S, Srivastava S, Tripathi RD, Trivedi PK (2008) Thiol metabolism and antioxidant systems complement each other during arsenate detoxification in Ceratophyllum demersum L. Aquat Toxicol 86:205–215

    CAS  PubMed  Google Scholar 

  50. Navrot N, Rouhier N, Gelhaye E, Jacquot JP (2007) Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol Plantarum 129(1):185–195

    CAS  Google Scholar 

  51. Ninkovic V (2003) Volatile communication between barley plants affects biomass allocation. J Exp Bot 54(389):1931–1939

    CAS  PubMed  Google Scholar 

  52. Ninkovic V, Dahlin I, Vucetic A, Petrovic-Obradovic O, Glinwood R, Webster B (2013) Volatile exchange between undamaged plants - a new mechanism affecting insect orientation in intercropping. PLoS One 8(7):e69431

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Pinto-Zevallos DM, Hellén H, Hakola H, Nouhuys SV, Holopainen JK (2013) Induced defenses of Veronica spicata: variability in herbivore-induced volatile organic compounds. Phytochem Lett 6(4):653–656

    CAS  Google Scholar 

  54. Qin S, Li J, Chen HH, Zhao GZ, Zhu WY, Jiang CL, Li WJ (2009) Rare actinobacteria from medicinal plants of tropical rainforests, Xishuangbanna: isolation, diversity and antimicrobial activity. Appl Environ Microb 75(19):6176–6186

    CAS  Google Scholar 

  55. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Google Scholar 

  56. Sanguin H, Sarniguet A, Gazengel K, Moënne-Loccoz Y, Grundmann GL (2009) Rhizosphere bacterial communities associated with disease suppressiveness stages of take‐all decline in wheat monoculture. New Phytol 184(3):694–707

    CAS  PubMed  Google Scholar 

  57. Selvakumar G, Panneerselvam P, Ganeshamurthy AN, Maheshwari DK (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Maheshwari DK (ed) Bacteria in agrobiology: Stress management. Springer, New York, pp 205–224

    Google Scholar 

  58. Sharma M, Sharma V, Tripathi BN (2016) Rapid activation of catalase followed by citrate efflux effectively improves aluminum tolerance in the roots of chick pea (Cicer arietinum). Protoplasma 253(3):709–718

    CAS  PubMed  Google Scholar 

  59. Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fert Soils 51(5):553–562

    CAS  Google Scholar 

  60. Srivastava MP, Sharma N (2011) Antimicrobial activities of Basidiocarp of some basidiomycetes strains against bacteria and fungi. J Mycol Pl Pathol 41:332–333

    Google Scholar 

  61. Stein SE (1999) An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J Am Soc Mass Spectrom 10:770–781

    CAS  Google Scholar 

  62. Tao S, Xu FL, Wang XJ, Liu WX, Gong ZM, Fang JY et al (2005) Organochlorine pesticides in agricultural soil and vegetables from Tianjin, China. Environ Sci Technol 39(8):2494–2499

    CAS  PubMed  Google Scholar 

  63. Theunissen J, Schelling G (1996) Pest and disease management by intercropping: suppression of thrips and rust in leek. Int J Pest Manage 42(4):227–234

    Google Scholar 

  64. Tholl D, Boland W, Hansel A, Loreto F, Röse US, Schnitzler JP (2006) Practical approaches to plant volatile analysis. Plant J 45(4):540–560

    CAS  PubMed  Google Scholar 

  65. Turlings TC, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11(2):122–129

    Google Scholar 

  66. Wallenstein MD (2017) Managing and manipulating the rhizosphere microbiome for plant health: a systems approach. Rhizosphere 3:230–232

    Google Scholar 

  67. Wang B, Li R, Ruan Y, Ou Y, Zhao Y, Shen Q (2015) Pineapple–banana rotation reduced the amount of Fusarium oxysporum more than maize–banana rotation mainly through modulating fungal communities. Soil Biol Biochem 86:77–86

    CAS  Google Scholar 

  68. Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, Shen Q (2017) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207

    CAS  Google Scholar 

  69. Yuan JS, Himanen SJ, Holopainen JK et al (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331

    PubMed  Google Scholar 

  70. Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe In 25(2):139–150

    CAS  Google Scholar 

  71. Zhao SC, Li KJ, Zhou W, Qiu SJ, Huang SW, He P (2016) Changes in soil microbial community, enzyme activities and organic matter fractions under long-term straw return in north-central China. Agr Ecosyst Environ 216:82–88

    CAS  Google Scholar 

  72. Zhou X, Wu F (2012) Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiol Ecol 80(2):469–478

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Prof. Wietse de Boer at the Netherlands Institute of Ecology (NIOO-KNAW) for help during the preparation of the manuscript, and colleagues from our research group (others than the authors) for assistance in conducting the field experiments. This study was supported by the National Natural Science Foundation of China (41671306, 41371290); the Excellent Youth Foundation of Jiangsu Province (BK20190040); China Agriculture Research System (CARS-13).

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X.L. and X.W. conceived the project and designed the study; Y.Z. conducted the experiments; X.L. and Z.Y. analyzed the data with assistance from X.W. and C.D.; X.L. and Z.Y. contributed to the drafting of the initial manuscript; all co-authors revised, read, and approved the final manuscript.

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Correspondence to Xingxiang Wang.

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Li, X., Yang, Z., Zhang, Y. et al. Atractylodes lancea volatiles induce physiological responses in neighboring peanut plant during intercropping. Plant Soil 453, 409–422 (2020). https://doi.org/10.1007/s11104-020-04615-z

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Keywords

  • Plant volatile
  • Physiological response
  • Root exudate
  • Rhizosphere microbial community