Plant and Soil

, Volume 391, Issue 1–2, pp 253–264 | Cite as

The response of root-associated bacterial community to the grafting of watermelon

  • Ning Ling
  • Yang Song
  • Waseem Raza
  • Qiwei Huang
  • Shiwei Guo
  • Qirong Shen
Regular Article


Background and aims

Grafting is commonly used to overcome soil-borne disease but how it affects the root-associated microbiome of concerned crops and the linkage between the microbiome and the resistance of soil-borne disease remain unknown. This study addressed the variation in the microbial activity and bacterial community in the rhizosphere of own-root bottle gourd (rootstock), own-root watermelon, and grafted-root watermelon under field conditions and tried to clarify how bacterial communities in the rhizosphere responded to grafting of watermelon.


Seven types of soil enzyme activities were tested by microplate fluorometric assay, and the root-associated bacterial community was compared using 454 pyrosequencing.


Clear distinctions in microbial activity and taxonomic levels between the different treatments were obtained. Compared with grafted-root watermelon, ungrafted watermelon recruited significantly higher beneficial bacterial genera, such as Bacillus spp. and Paenibacillus spp., suggesting the grafted watermelon root could not have the ability to harbor highly beneficial bacteria to exert soil-borne disease resistance. However, a significantly higher Shannon-Wiener index at any reads level was found in the rhizosphere of grafted watermelon compared with ungrafted watermelon.


Root-associated bacteria of grafted watermelon possess a broader niche overlap which would provide the potential to exclude the pathogen challenge. We proposed that the grafted watermelon might exert soil-borne disease resistance by maximizing the niche occupancy of rhizosphere rather than by recruiting more beneficial bacteria.


Grafting Watermelon Soil enzyme Bacterial community 454 Pyrosequencing 



Financial supports from the National Basic Research Program of China (2015CB150503), Natural Science Foundation of China (31301853) and from the Fundamental Research Funds for the Central Universities (KYZ201307) are acknowledged. Many graduate students and staffs involved in maintaining the field plots and collecting soil samples but not listed as coauthors are grateful.


  1. Ai C, Liang G, Sun J, Wang X, Zhou W (2012) Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 173–174:330–338CrossRefGoogle Scholar
  2. Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM (2005) Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434:217–221CrossRefPubMedGoogle Scholar
  3. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486CrossRefPubMedGoogle Scholar
  4. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13CrossRefPubMedGoogle Scholar
  5. Chaer G, Fernandes M, Myrold D, Bottomley P (2009) Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils. Microb Ecol 58:414–424CrossRefPubMedGoogle Scholar
  6. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499CrossRefGoogle Scholar
  7. Colla G, Rouphael Y, Cardarelli M, Salerno A, Rea E (2010) The effectiveness of grafting to improve alkalinity tolerance in watermelon. Environ Exp Bot 68:283–291CrossRefGoogle Scholar
  8. Cook RJ, Thomashow LS, Weller DM, Fujimoto D, Mazzola M, Bangera G, Kim DS (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci U S A 92:4197–4201CrossRefPubMedCentralPubMedGoogle Scholar
  9. Deng S, Kang H, Freeman C (2011) Microplate fluorimetric assay of soil enzymes. In: Dick RP (ed) Methods in soil enzymology. Soil Science Society of America, Madison, pp 311–318Google Scholar
  10. Deng S, Popova IE, Dick L, Dick R (2013) Bench scale and microplate format assay of soil enzyme activities using spectroscopic and fluorometric approaches. Appl Soil Ecol 64:84–90CrossRefGoogle Scholar
  11. Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280CrossRefPubMedCentralPubMedGoogle Scholar
  12. Garbeva P, Postma J, van Veen JA, van Elsas JD (2006) Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environ Microbiol 8:233–246CrossRefPubMedGoogle Scholar
  13. Garbeva P, Elsas JD, Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32CrossRefGoogle Scholar
  14. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520CrossRefPubMedGoogle Scholar
  15. Huse SM, Dethlefsen L, Huber JA, Mark Welch D, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255CrossRefPubMedCentralPubMedGoogle Scholar
  16. Kotroczó Z, Veres Z, Fekete I, Krakomperger Z, Tóth JA, Lajtha K, Tóthmérész B (2014) Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol Biochem 70:237–243CrossRefGoogle Scholar
  17. Lee J-M (1994) Cultivation of grafted vegetables I. Current status, grafting methods, and benefits. Hortscience 29:235–239Google Scholar
  18. Lellei-Kovács E, Kovács-Láng E, Botta-Dukát Z, Kalapos T, Emmett B, Beier C (2011) Thresholds and interactive effects of soil moisture on the temperature response of soil respiration. Eur J Soil Biol 47:247–255CrossRefGoogle Scholar
  19. Li X-G, Zhang T-L, Wang X-X, Hua K, Zhao L, Han Z-M (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 9:164–173Google Scholar
  20. Ling N, Huang Q, Guo S, Shen Q (2011) Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f.sp. niveum. Plant Soil 341:485–493CrossRefGoogle Scholar
  21. Ling N, Deng K, Song Y, Wu Y, Zhao J, Raza W, Huang Q, Shen Q (2013a) Variation of rhizosphere bacterial community in watermelon continuous mono-cropping soil by long-term application of a novel bioorganic fertilizer. Microbiol Res 169:570–578CrossRefPubMedGoogle Scholar
  22. Ling N, Zhang W, Wang D, Mao J, Huang Q, Guo S, Shen Q (2013b) Root exudates from grafted-root watermelon showed a certain contribution in inhibiting Fusarium oxysporum f. sp. niveum. PLoS One 8:e63383CrossRefPubMedCentralPubMedGoogle Scholar
  23. Liu N, Zhou B, Zhao X, Lu B, Li Y, Hao J (2009) Grafting eggplant onto tomato rootstock to suppress Verticillium dahliae infection: the effect of root exudates. Hortscience 44:2058–2062Google Scholar
  24. Mazzola M (2004) Assessment and management of soil microbial community structure for disease suppression. Annu Rev Phytopathol 42:35–59CrossRefPubMedGoogle Scholar
  25. McSpadden Gardener BB (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94:1252–1258CrossRefPubMedGoogle Scholar
  26. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100CrossRefPubMedGoogle Scholar
  27. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762CrossRefGoogle Scholar
  28. Nguyen C (2009) Rhizodeposition of organic C by plant: mechanisms and controls. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer, Netherlands, pp 97–123CrossRefGoogle Scholar
  29. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596CrossRefPubMedCentralPubMedGoogle Scholar
  30. Rouphael Y, Schwarz D, Krumbein A, Colla G (2010) Impact of grafting on product quality of fruit vegetables. Sci Hortic-Amsterdam 127:172–179CrossRefGoogle Scholar
  31. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556CrossRefPubMedCentralPubMedGoogle Scholar
  32. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefPubMedCentralPubMedGoogle Scholar
  33. Spohn M, Kuzyakov Y (2013) Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation—coupling soil zymography with 14C imaging. Soil Biol Biochem 67:106–113CrossRefGoogle Scholar
  34. Thies JA, Ariss JJ, Hassell RL, Olson S, Kousik CS, Levi A (2010) Grafting for management of southern root-knot nematode, meloidogyne incognita, in watermelon. Plant Dis 94:1195–1199CrossRefGoogle Scholar
  35. Turhan A, Ozmen N, Kuscu H, Serbeci MS, Seniz V (2012) Influence of rootstocks on yield and fruit characteristics and quality of watermelon. Hortic Environ Biotechnol 53:336–341CrossRefGoogle Scholar
  36. Turner BL, Hopkins DW, Haygarth PM, Ostle N (2002) β-glucosidase activity in pasture soils. Appl Soil Ecol 20:157–162CrossRefGoogle Scholar
  37. Viebahn M, Veenman C, Wernars K, van Loon LC, Smit E, Bakker PA (2005) Assessment of differences in ascomycete communities in the rhizosphere of field-grown wheat and potato. FEMS Microbiol Ecol 53:245–253CrossRefPubMedGoogle Scholar
  38. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve bayesian classifier for rapid assignment of rrna sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedCentralPubMedGoogle Scholar
  39. Wu H-S, Raza W, Fan J-Q, Sun Y-G, Bao W, Liu D-Y, Huang Q-W, Z-s M, Shen Q-R, Miao W-G (2008) Antibiotic effect of exogenously applied salicylic acid on in vitro soilborne pathogen, Fusarium oxysporum f.sp.niveum. Chemosphere 74:45–50CrossRefPubMedGoogle Scholar
  40. Wu F, Liu B, Zhou X (2010) Effects of root exudates of watermelon cultivars differing in resistance to Fusarium wilt on the growth and development of Fusarium oxysporum f.sp. niveum. Allelopathy J 25:403–414Google Scholar
  41. Xu Z, Shao J, Li B, Yan X, Shen Q, Zhang R (2013) Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl Environ Microbiol 79:808–815CrossRefPubMedCentralPubMedGoogle Scholar
  42. Yetisir H, Sari N, Yucel S (2003) Rootstock resistance to Fusarium wilt and effect on watermelon fruit yield and quality. Phytoparasitica 31:163–169CrossRefGoogle Scholar
  43. Zhao J, Zhang R, Xue C, Xun W, Sun L, Xu Y, Shen Q (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443–453CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ning Ling
    • 1
    • 2
  • Yang Song
    • 1
    • 2
  • Waseem Raza
    • 1
    • 2
  • Qiwei Huang
    • 1
    • 2
  • Shiwei Guo
    • 1
    • 2
  • Qirong Shen
    • 1
    • 2
  1. 1.Jiangsu Key Laboratory for Solid Organic Waste UtilizationNanjing Agricultural UniversityNanjingChina
  2. 2.Jiangsu Provincial Coordinated Research Center for Organic Solid Waste UtilizationNanjing Agricultural UniversityNanjingChina

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