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Plant Grafting Shapes Complexity and Co-occurrence of Rhizobacterial Assemblages

  • Plant Microbe Interactions
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Abstract

Grafting is a basic technique which is widely used to increase yield and enhance biotic and abiotic stress tolerance in plant production. The diversity and interactions of rhizobacterial assemblages shaped by grafting are important for the growth of their hosts but remain poorly understood. To test the hypothesis that plant grafting shapes complexity and co-occurrence of rhizobacterial assemblage, four types of plants, including ungrafted bottle gourd (B), ungrafted watermelon (W), grafted watermelon with bottle gourd rootstock (W/B), and grafted bottle gourd with watermelon rootstock (B/W), were cultivated in two soil types in a greenhouse, and the rhizosphere bacterial communities were analyzed by 16S rRNA gene high-throughput sequencing. Both the soil type and grafting significantly influenced the bacterial community composition. Grafting increased bacterial within-sample diversity in both soils. Core enriched operational taxonomic units (OTUs) in the W/B rhizosphere compared with the other three treatments (B, W, and B/W) were mainly affiliated with Alphaproteobacteria, Deltaproteobacteria, and Bacteroidetes, which are likely related to methanol oxidation, methylotrophy, fermentation, and ureolysis. Co-occurrence network analysis proved that grafting increased network complexity, including the number of nodes, edges, and modules. Moreover, grafting strengthened the structural robustness of the network in the rhizosphere, while ungrafted watermelon had the lowest network robustness. Homogeneous selection played a predominant role in bacterial community assembly, and the contribution of dispersal limitation was increased in grafted watermelon with bottle gourd rootstock. Grafting increased the diversity and transformed the network topology of the bacterial community, which indicated that grafting could improve species coexistence in the watermelon rhizosphere.

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References

  1. Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK, Johnson N (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19(8):926–936

    Article  Google Scholar 

  2. Kuzyakov Y, Razavi BS (2019) Rhizosphere size and shape: temporal dynamics and spatial stationarity. Soil Biol Biochem 135:343–360. https://doi.org/10.1016/j.soilbio.2019.05.011

    Article  CAS  Google Scholar 

  3. Nuccio EE, Starr E, Karaoz U, Brodie EL, Zhou J, Tringe SG, Malmstrom RR, Woyke T, Banfield JF, Firestone MK, Pett-Ridge J (2020) Niche differentiation is spatially and temporally regulated in the rhizosphere. ISME J 14:999–1014

    Article  CAS  Google Scholar 

  4. Ravanbakhsh M, Kowalchuk GA, Jousset A (2019) Root-associated microorganisms reprogram plant life history along the growth–stress resistance tradeoff. ISME J 13:3093–3101

    Article  CAS  Google Scholar 

  5. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112(8):E911–E920

    Article  CAS  Google Scholar 

  6. Pérez-Jaramillo JE, Carrión VJ, Bosse M, Ferrão LFV, de Hollander M, Garcia AAF, Ramírez CA, Mendes R, Raaijmakers JM (2017) Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits. ISME J 11:2244–2257. https://doi.org/10.1038/ismej.2017.85

    Article  PubMed  PubMed Central  Google Scholar 

  7. Wang J, Xue C, Song Y, Wang L, Huang Q, Shen Q (2016) Wheat and rice growth stages and fertilization regimes alter soil bacterial community structure, but not diversity. Front Microbiol 7:1207. https://doi.org/10.3389/fmicb.2016.01207

    Article  PubMed  PubMed Central  Google Scholar 

  8. Mendes LW, Raaijmakers JM, de Hollander M, Mendes R, Tsai SM (2017) Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME J 12:212–224. https://doi.org/10.1038/ismej.2017.158

    Article  PubMed  PubMed Central  Google Scholar 

  9. Guan W, Xin Z, Hassell R, Thies J (2012) Defense mechanisms involved in disease resistance of grafted vegetables. Hortscience 47(2):164–170. https://doi.org/10.21273/hortsci.47.2.164

    Article  CAS  Google Scholar 

  10. Marasco R, Rolli E, Fusi M, Michoud G, Daffonchio D (2018) Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome 6(1):3. https://doi.org/10.1186/s40168-017-0391-2

    Article  PubMed  PubMed Central  Google Scholar 

  11. Sharma A, Wang J, Xu D, Tao S, Chong S, Yan D, Li Z, Yuan H, Zheng B (2020) Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Sci Total Environ 713:1–13. https://doi.org/10.1016/j.scitotenv.2020.136675

    Article  CAS  Google Scholar 

  12. Warschefsky EJ, Klein LL, Frank MH, Chitwood DH, Londo JP, von Wettberg EJ, Miller AJ (2016) Rootstocks: diversity, domestication, and impacts on shoot phenotypes. Trends Plant Sci 21(5):418–437

    Article  CAS  Google Scholar 

  13. Poudel R, Jumpponen A, Kennelly MM, Rivard C, Gomez-Montano LA, Garrett K (2018) Rootstocks shape the rhizobiome: rhizosphere and endosphere bacterial communities in the grafted tomato system. Appl Environ Microbiol 85(2):e01765–e01718. https://doi.org/10.1128/AEM.01765-18

    Article  Google Scholar 

  14. Liu N, Yang J, Fu X, Zhang L, Tang K, Guy KM, Hu Z, Guo S, Xu Y, Zhang M (2016) Genome-wide identification and comparative analysis of grafting-responsive mRNA in watermelon grafted onto bottle gourd and squash rootstocks by high-throughput sequencing. Mol Gen Genomics 291:621–633. https://doi.org/10.1007/s00438-015-1132-5

    Article  CAS  Google Scholar 

  15. Ling N, Zhang W, Wang D, Mao J, Huang Q, Guo S, Shen Q (2013) Root exudates from grafted-root watermelon showed a certain contribution in inhibiting Fusarium oxysporum f. sp. niveum. PLoS One 8(5):e63383. https://doi.org/10.1371/journal.pone.0063383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Song Y, Zhu C, Raza W, Wang D, Huang Q, Guo S, Ling N, Shen Q (2016) Coupling of the chemical niche and microbiome in the rhizosphere: implications from watermelon grafting. Front Agric Sci Eng 3(3):249–262

    Article  Google Scholar 

  17. Toju H, Okayasu K, Notaguchi M (2019) Leaf-associated microbiomes of grafted tomato plants. Sci Rep 9:1787. https://doi.org/10.1038/s41598-018-38344-2

  18. Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576

    Article  CAS  Google Scholar 

  19. Konopka A, Lindemann S, Fredrickson J (2015) Dynamics in microbial communities: unraveling mechanisms to identify principles. ISME J 9(7):1488–1495. https://doi.org/10.1038/ismej.2014.251

    Article  PubMed  Google Scholar 

  20. Ling N, Song Y, Raza W, Huang Q, Guo S, Shen Q (2015) The response of root-associated bacterial community to the grafting of watermelon. Plant Soil 391(1–2):253–264. https://doi.org/10.1007/s1104-015-2399-3

  21. Song Y, Ling N, Ma J, Wang J, Zhu C, Raza W, Shen Y, Huang Q, Shen Q (2016) Grafting resulted in a distinct proteomic profile of watermelon root exudates relative to the un-grafted watermelon and the rootstock plant. J Plant Growth Regul 35(3):778–791

    Article  CAS  Google Scholar 

  22. Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58. https://doi.org/10.1186/s40168-018-0445-0

    Article  PubMed  PubMed Central  Google Scholar 

  23. Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23(1):25–41. https://doi.org/10.1016/j.tplants.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  24. Liu W, Ling N, Guo J, Ruan Y, Guo S (2020) Legacy effects of 8-year nitrogen inputs on bacterial assemblage in wheat rhizosphere. Biol Fertil Soils 1–14. https://doi.org/10.1007/s00374-020-01435-2

  25. Garcia-Lozano M, Dutta SK, Pet N, Tomason YR, Lopez C, Katam R, Levi A, Nimmakayala P, Reddy UK (2020) Transcriptome changes in reciprocal grafts involving watermelon and bottle gourd reveal molecular mechanisms involved in increase of the fruit size, rind toughness and soluble solids. Plant Mol Biol 102:213–223. https://doi.org/10.1007/s1103-019-00942-7

    Article  CAS  PubMed  Google Scholar 

  26. Li Y, Tang K, Zhang L, Zhao Z, Xie X, Chen C-TA, Wang D, Jiao N, Zhang Y (2018) Coupled carbon, sulfur, and nitrogen cycles mediated by microorganisms in the water column of a shallow-water hydrothermal ecosystem. Front Microbiol 9:2718. https://doi.org/10.3389/fmicb.2018.02718

    Article  PubMed  PubMed Central  Google Scholar 

  27. Li H, Wang J, Liu Q, Zhou Z, Chen F, Xiang D (2019) Effects of consecutive monoculture of sweet potato on soil bacterial community as determined by pyrosequencing. J Basic Microbiol 59:181–191. https://doi.org/10.1002/jobm.201800304

    Article  CAS  PubMed  Google Scholar 

  28. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  Google Scholar 

  29. Feng K, Zhang Z, Cai W, Liu W, Xu M, Yin H, Wang A, He Z, Deng Y (2017) Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol Ecol 26(21):6170–6182

    Article  Google Scholar 

  30. Kong Y, Ling N, Xue C, Chen H, Ruan Y, Guo J, Zhu C, Wang M, Shen Q, Guo S (2019) Long-term fertilization regimes change soil nitrification potential by impacting active autotrophic ammonia oxidizers and nitrite oxidizers as assessed by DNA stable isotope probing. Environ Microbiol 21(4):1224–1240

    Article  CAS  Google Scholar 

  31. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  Google Scholar 

  32. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44(Web Server issue):W242–W245

    Article  CAS  Google Scholar 

  33. Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinforma 13(1):113. https://doi.org/10.1186/1471-2105-13-113

    Article  Google Scholar 

  34. Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. In: Proc Int AAAI Conf Weblogs Soc Media. https://www.aaai.org/ocs/index.php/ICWSM/09/paper/viewPaper/154

  35. Peng GS, Wu J (2016) Optimal network topology for structural robustness based on natural connectivity. Physica A 443:212–220

    Article  Google Scholar 

  36. Feng Y, Chen R, Stegen JC, Guo Z, Zhang J, Li Z, Lin X (2018) Two key features influencing community assembly processes at regional scale: initial state and degree of change in environmental conditions. Mol Ecol 27(24):5238–5251. https://doi.org/10.1111/mec.14914

    Article  PubMed  Google Scholar 

  37. Chialva M, Fossalunga ASD, Daghino S, Ghignone S, Bagnaresi P, Chiapello M, Novero M, Spadaro D, Perotto S, Bonfante P (2018) Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol 220(4):1296–1308

    Article  CAS  Google Scholar 

  38. Wang J, Jiang L, Wu R (2017) Plant grafting: how genetic exchange promotes vascular reconnection. New Phytol 214(1):56–65. https://doi.org/10.1111/nph.14383

    Article  PubMed  Google Scholar 

  39. Gaion LA, Braz LT, Carvalho RF (2018) Grafting in vegetable crops: a great technique for agriculture. Int J Veg Sci 24(1):85–102. https://doi.org/10.1080/19315260.2017.1357062

    Article  Google Scholar 

  40. Maynard DS, Crowther TW, Bradford MA (2017) Competitive network determines the direction of the diversity–function relationship. Proc Natl Acad Sci USA 114(43):11464–11469

    Article  CAS  Google Scholar 

  41. Wei Z, Yang T, Friman V, Xu Y, Shen Q, Jousset A (2015) Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun 6:8413–8421

    Article  CAS  Google Scholar 

  42. Hu J, Wei Z, Friman V-P, Gu S, Wang X, Eisenhauer N, Yang T, Ma J, Shen Q, Xu Y, Jousset A (2016) Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. MBio 7:e01790–e01716

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA 109(4):1159–1164

    Article  Google Scholar 

  44. Berendsen RL, van Verk MC, Stringlis IA, Zamioudis C, Tommassen J, Pieterse CMJ, Bakker PAHM (2015) Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genomics 16:539. https://doi.org/10.1186/s12864-015-1632-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, Sa T (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8(705). https://doi.org/10.3389/fpls.2017.00705

  46. Subramanian P, Kim K, Krishnamoorthy R, Mageswari A, Selvakumar G, Sa T (2016) Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. PLoS One 11(8):e0161592. https://doi.org/10.1371/journal.pone.0161592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lu Y, Wang L, Xue Y, Zhang C, Xing X, Lou K, Zhang Z, Li Y, Zhang G, Bi J, Su Z (2009) Production of violet pigment by a newly isolated psychrotrophic bacterium from a glacier in Xinjiang, China. Biochem Eng J 43(2):135–141. https://doi.org/10.1016/j.bej.2008.09.009

    Article  CAS  Google Scholar 

  48. Ambrožič Avguštin J, Žgur Bertok D, Kostanjšek R, Avguštin G (2013) Isolation and characterization of a novel violacein-like pigment producing psychrotrophic bacterial species Janthinobacterium svalbardensis sp. nov. Anton Leeuw Int J G 103:763–769. https://doi.org/10.1007/s10482-012-9858-0

    Article  CAS  Google Scholar 

  49. Layeghifard M, Hwang DM, Guttman DS (2017) Disentangling interactions in the microbiome: a network perspective. Trends Microbiol 25(3):217–228

    Article  CAS  Google Scholar 

  50. Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MGA (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun 10(1):4841. https://doi.org/10.1038/s41467-019-12798-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Munoz R, Teeling H, Amann R, Rossello-Mora R (2020) Ancestry and adaptive radiation of Bacteroidetes as assessed by comparative genomics. Syst Appl Microbiol 43(2):126065. https://doi.org/10.1016/j.syapm.2020.126065

    Article  CAS  PubMed  Google Scholar 

  52. Radka C, Frank M, Rock C, Yao J (2020) Fatty acid activation and utilization by Alistipes finegoldii, a representative Bacteroidetes resident of the human gut microbiome. Mol Microbiol 00:1–19. https://doi.org/10.1111/mmi.14445

    Article  CAS  Google Scholar 

  53. Trujillo ME (2016) In: eLS (ed) Actinobacteria. John Wiley & Sons, Ltd. https://doi.org/10.1002/9780470015902.a0020366.pub2

  54. Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, Jousset A, 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

    Article  CAS  Google Scholar 

  55. Palaniyandi SA, Yang SH, Zhang L, Suh J-W (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Environ Microbiol 97(22):9621–9636

    CAS  Google Scholar 

  56. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332(6033):1097–1100

    Article  CAS  Google Scholar 

  57. Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio 2:e00122–e00111

    Article  Google Scholar 

  58. Herren CM, Mcmahon KD (2018) Keystone taxa predict compositional change in microbial communities. Environ Microbiol 20(6):2207–2217

    Article  Google Scholar 

  59. Chen L, Jiang Y, Liang C, Luo Y, Sun B (2019) Competitive interaction with keystone taxa induced negative priming under biochar amendments. Microbiome 7(77):77. https://doi.org/10.1186/s40168-019-0693-7

    Article  PubMed  PubMed Central  Google Scholar 

  60. Zhou J, Ning D (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev 81(4):e00002–e00017. https://doi.org/10.1128/MMBR.00002-17

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We are thankful to Chen Zhu and Yang Song for their assistance with the DNA extraction and bio-informatic analysis and also to the staff of the Nanjing Institute of Vegetable Science for providing seedlings.

Funding

This study was supported by the National Nature Science Foundation of China (31772398), the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56), and the Fundamental Research Funds for the Central Universities (KYT201802).

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Ruan, Y., Wang, T., Guo, S. et al. Plant Grafting Shapes Complexity and Co-occurrence of Rhizobacterial Assemblages. Microb Ecol 80, 643–655 (2020). https://doi.org/10.1007/s00248-020-01532-7

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