Skip to main content

Advertisement

SpringerLink
Log in

Phosphorus Input Alters the Assembly of Rice (Oryza sativa L.) Root-Associated Communities

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Rice root–associated microbial community play an important role in plant nutrient acquisition, biomass production, and stress tolerance. Herein, root-associated community assembly was investigated under different phosphate input levels in phosphorus (P)-deficient paddy soil. Rice was grown in a long-term P-depleted paddy soil with 0 (P0), 50 (PL), or 200 (PH) mg P2O5 kg−1 application. DNA from root endophytes was isolated after 46 days, and PCR amplicons from archaea, bacteria, and fungi were sequenced by an Illumina Miseq PE300 platform, respectively. P application had no significant effect on rice root endophytic archaea, which were dominated by ammonia-oxidizing Candidatus Nitrososphaera. By contrast, rice root endophytic community structure of the bacteria and fungi was affected by soil P. Low P input increased endophytic bacterial diversity, whereas high P input increased rhizosphere fungi diversity. Bacillus and Pleosporales, associated with phosphate solubilization and P uptake, dominated in P0 and PH treatments, and Pseudomonas were more abundant in the PL treatment than in the P0 and PH treatments. Co-occurrence network analysis revealed a close interaction between endophytic bacteria and fungi. Soil P application affected both the rice root endosphere and soil rhizosphere microbial community and interaction between rice root endophytic bacteria, and fungi, especially species related to P cycling.

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

Similar content being viewed by others

References

  1. Arora J, Ramawat KG (2017) An introduction to endophytes. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, vol 1. Springer International Publishing, Cham, pp 1–23

    Google Scholar 

  2. Hardoim PR, van Overbeek LS, Berg G, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798. https://doi.org/10.1016/j.chembiol.2012.06.004

    Article  CAS  PubMed  Google Scholar 

  4. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  5. Lamb TG, Tonkyn DW, Kluepfel DA (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120. https://doi.org/10.1139/m96-143

    Article  CAS  Google Scholar 

  6. Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572

    Article  PubMed  Google Scholar 

  7. Jain P, Pundir RK (2017) Potential role of endophytes in sustainable agriculture-recent developments and future prospects. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, vol 1. Springer International Publishing, Cham, pp 145–169

    Chapter  Google Scholar 

  8. Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, Bokulich NA, Mills DA, Martin G, Taghavi S, van der Lelie D, Gilbert JA, Jansson JK (2015) The soil microbiome influences grapevine-associated microbiota. mBio 6:e02527–e02514. https://doi.org/10.1128/mBio.02527-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Liu YL, Ge TD, Zhu ZK, Liu SL, Luo Y, Li Y, Wang P, Gavrichkova O, Xu XL, Wang JK, Wu JS, Guggenberger G, Kuzyakov Y (2019) Carbon input and allocation by rice into paddy soils: a review. Soil Biol Biochem 133:97–107. https://doi.org/10.1016/j.soilbio.2019.02.019

    Article  CAS  Google Scholar 

  10. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823. https://doi.org/10.1371/journal.pone.0014823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zhang XX, Gao JS, Cao YH, Ma XT, He JZ (2013) Long-term rice and green manure rotation alters the endophytic bacterial communities of the rice root. Microb Ecol 66:917–926. https://doi.org/10.1007/s00248-013-0293-1

    Article  PubMed  Google Scholar 

  12. Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, Van Elsas JD (2011) Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154–164. https://doi.org/10.1111/j.1574-6941.2011.01092.x

    Article  CAS  PubMed  Google Scholar 

  13. Wei XM, Zhu ZK, Wei L, Wu JH, Ge TD (2019) Biogeochemical cycles of key elements in the paddy-rice rhizosphere: microbial mechanisms and coupling processes. Rhizosphere 10:100145. https://doi.org/10.1016/j.rhisph.2019.100145

    Article  Google Scholar 

  14. Wu XH, Ge TD, Yan WD, Zhou J, Wei XM, Chen L, Chen XB, Nannipieri P, Wu JS (2017) Irrigation management and phosphorus addition alter the abundance of carbon dioxide-fixing autotrophs in phosphorus-limited paddy soil. FEMS Microbiol Ecol 93:fix154. https://doi.org/10.1093/femsec/fix154

    Article  CAS  Google Scholar 

  15. Wei X, Hu Y, Peng P, Zhu ZK, Atere CT, O’Donnell AG, Wu JS, Ge TD (2017) Effect of P stoichiometry on the abundance of nitrogen-cycle genes in phosphorus-limited paddy soil. Biol Fertil Soils 53:767–776. https://doi.org/10.1007/s00374-017-1221-1

    Article  CAS  Google Scholar 

  16. Long XE, Yao HY, Huang Y, Wei WX, Zhu YG (2018) Phosphate levels influence the utilisation of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil. Soil Biol Biochem 118:103–114. https://doi.org/10.1016/j.soilbio.2017.12.014

    Article  CAS  Google Scholar 

  17. Li YY, Pan FX, Yao HY (2019) Response of symbiotic and asymbiotic nitrogen-fixing microorganisms to nitrogen fertilizer application. J Soils Sediments 19:1948–1958. https://doi.org/10.1007/s11368-018-2192-z

    Article  CAS  Google Scholar 

  18. Bruce A, Smith SE, Tester M (1994) The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytol 127:507–514. https://doi.org/10.1111/j.1469-8137.1994.tb03968.x

    Article  Google Scholar 

  19. Sylvia DM, Neal LH (1990) Nitrogen affects the phosphorus response of VA mycorrhiza. New Phytol 115:303–310. https://doi.org/10.1111/j.1469-8137.1990.tb00456.x

    Article  CAS  PubMed  Google Scholar 

  20. Sun L, Qiu FB, Zhang XX, Dai X, Dong XZ, Song W (2008) Endophytic bacterial diversity in rice (Oryza sativa L) roots estimated by 16S rDNA sequence analysis. Microb Ecol 55:415–424. https://doi.org/10.1007/s00248-007-9287-1

    Article  CAS  PubMed  Google Scholar 

  21. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinf 27:863–864. https://doi.org/10.1093/bioinformatics/btr026

    Article  CAS  Google Scholar 

  22. Zhang J, Kobert K, Flouri T, Stamatakis A (2013) PEAR: a fast and accurate Illumina Paired-End reAd merger. Bioinf 30:614–620. https://doi.org/10.1093/bioinformatics/btt593

    Article  CAS  Google Scholar 

  23. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Steven MHH, Wagner H (2014) Vegan: Community Ecology Package R package version 22-0 https://CRANR-project.org/package=vegan

  26. Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8:e1002687. https://doi.org/10.1371/journal.pcbi.1002687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. In: Hamacher M, Eisenacher M, Stephan C (eds) Data mining in proteomics: from standards to applications. Humana Press, Totowa, pp 291–303

    Chapter  Google Scholar 

  28. Morris JH, Apeltsin L, Newman AM, Baumbach J, Wittkop T, Su G, Bader GD, Ferrin TE (2011) clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinf 12:436. https://doi.org/10.1186/1471-2105-12-436

    Article  CAS  Google Scholar 

  29. Su G, Kuchinsky A, Morris JH, States DJ, Meng F (2010) GLay: community structure analysis of biological networks. Bioinf 26:3135–3137. https://doi.org/10.1093/bioinformatics/btq596

    Article  CAS  Google Scholar 

  30. Newman MEJ, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E Stat Nonlinear Soft Matter Phys 69:026113. https://doi.org/10.1103/PhysRevE.69.026113

    Article  CAS  Google Scholar 

  31. Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2011) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36. https://doi.org/10.1094/MPMI-08-11-0204

    Article  CAS  Google Scholar 

  32. Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10:1978–1987. https://doi.org/10.1111/j.1462-2920.2008.01613.x

    Article  CAS  PubMed  Google Scholar 

  33. Müller H, Berg C, Landa BB, Auerbach A, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front Microbiol 6:138. https://doi.org/10.3389/fmicb.2015.00138

    Article  PubMed  PubMed Central  Google Scholar 

  34. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869. https://doi.org/10.1111/j.1574-6976.2009.00179.x

    Article  CAS  PubMed  Google Scholar 

  35. Tang YQ, Zhang XY, Li DD, Wang HM, Chen FS, Fu XL, Fang XM, Sun XM, Yu GR (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol Biochem 103:284–293. https://doi.org/10.1016/j.soilbio.2016.09.001

    Article  CAS  Google Scholar 

  36. Großkopf R, Stubner S, Liesack W (1998) Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl Environ Microbiol 64:4983–4989

    Article  PubMed Central  Google Scholar 

  37. Ahn JH, Song J, Kim BY, Kim MS, Joa JH, Weon HY (2012) Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J Microbiol 50:754–765. https://doi.org/10.1007/s12275-012-2409-6

    Article  PubMed  Google Scholar 

  38. Goux X, Calusinska M, Fossépré M, Benizri E, Delfosse P (2016) Start-up phase of an anaerobic full-scale farm reactor-Appearance of mesophilic anaerobic conditions and establishment of the methanogenic microbial community. Bioresour Technol 212:217–226. https://doi.org/10.1016/j.biortech.2016.04.040

    Article  CAS  PubMed  Google Scholar 

  39. Winkel M, Mitzscherling J, Overduin PP, Horn F, Winterfeld M, Rijkers R, Grigoriev MN, Knoblauch C, Mangelsdorf K, Wagner D, Liebner S (2018) Anaerobic methanotrophic communities thrive in deep submarine permafrost. Sci Rep 8:1291. https://doi.org/10.1038/s41598-018-19505-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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 U S A 112:E911–E920. https://doi.org/10.1073/pnas.1414592112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wang WF, Zhai YY, Cao LX, Tan HM, Zhang RD (2016) Endophytic bacterial and fungal microbiota in sprouts, roots and stems of rice (Oryza sativa L). Microbiol Res 188–189:1–8. https://doi.org/10.1016/j.micres.2016.04.009

    Article  PubMed  Google Scholar 

  42. Hameed A, Yeh MW, Hsieh YT, Chung WC, Lo CT, Young LS (2015) Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil 394:177–197. https://doi.org/10.1007/s11104-015-2506-5

    Article  CAS  Google Scholar 

  43. Okunishi S, Sako K, Mano H, Imamura A, Morisaki H (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ 20:168–177. https://doi.org/10.1264/jsme2.20.168

    Article  Google Scholar 

  44. Wei XM, Hu YJ, Razavi BS, Zhou J, Shen JL, Nannipieri P, Wu JH, Ge TD (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70. https://doi.org/10.1016/j.soilbio.2018.12.025

    Article  CAS  Google Scholar 

  45. Walia A, Guleria S, Chauhan A, Mehta P (2017) Endophytic bacteria: role in phosphate solubilization. In: Maheshwari DK, Annapurna K (eds) Endophytes: crop productivity and protection, vol 2. Springer International Publishing, Cham, pp 61–93

    Chapter  Google Scholar 

  46. Panhwar QA, Radziah O, Naher UA, Zaharah AR, Sariah M (2012) Root colonization and association of phosphate-solubilizing bacteria at various levels of triple supper phosphate in aerobic rice seedlings. Afr J Microbiol Res 6:2277–2286. https://doi.org/10.5897/AJMR11.916

    Article  CAS  Google Scholar 

  47. Naher UA, Radziah O, Halimi MS, Shamsuddin ZH, Mohd Razi I (2008) Effect of inoculation on root exudates carbon sugar and amino acids production of different rice varieties. Res J Microbiol 3:580–587 https://scialert.net/abstract/?doi=jm.2008.580.587

    Article  Google Scholar 

  48. Vallino M, Greppi D, Novero M, Bonfante P, Lupotto E (2009) Rice root colonisation by mycorrhizal and endophytic fungi in aerobic soil. Ann Appl Biol 154:195–204. https://doi.org/10.1111/j.1744-7348.2008.00286.x

    Article  Google Scholar 

  49. Panneerselvam P, Kumar U, Sugitha TCK, Parameswaran C, Sahoo S, Binodh AK, Jahan A, Anandan A (2017) Arbuscular mycorrhizal fungi (AMF) for sustainable rice production. In: Adhya TK, Mishra BB, Annapurna K et al (eds) Advances in soil microbiology: recent trends and future prospects, vol 2. Soil-Microbe-Plant Interaction Springer Singapore, Singapore, pp 99–126

    Chapter  Google Scholar 

  50. Pili NN, França SC, Kyndt T, Makumba BA, Skilton R, Höfte M, Mibey RK, Gheysen G (2016) Analysis of fungal endophytes associated with rice roots from irrigated and upland ecosystems in Kenya. Plant Soil 405:371–380. https://doi.org/10.1007/s11104-015-2590-6

    Article  CAS  Google Scholar 

  51. Potshangbam M, Devi SI, Sahoo D, Strobel GA (2017) Functional characterization of endophytic fungal community associated with Oryza sativa L and Zea mays L. Front Microbiol 8:325. https://doi.org/10.3389/fmicb.2017.00325

    Article  PubMed  PubMed Central  Google Scholar 

  52. Vergara C, Araujo KEC, Alves LS, Souza SR, Santos LA, Santa-Catarina C, Silva K, Pereira GMD, Xavier GR, Zilli JÉ (2018) Contribution of dark septate fungi to the nutrient uptake and growth of rice plants. Braz J Microbiol 49:67–78. https://doi.org/10.1016/j.bjm.2017.04.010

    Article  CAS  PubMed  Google Scholar 

  53. Liu M, Liu J, Chen XF, Jiang CY, Wu M, Li ZP (2018) Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus. Biol Fertil Soils 54:259–267. https://doi.org/10.1007/s00374-017-1258-1

    Article  CAS  Google Scholar 

  54. Tian XL, Cao LX, Tan HM, Zeng QG, Jia YY, Han WQ, Zhou SN (2004) Study on the communities of endophytic fungi and endophytic actinomycetes from rice and their antipathogenic activities in vitro. World J Microbiol Biotechnol 20:303–309. https://doi.org/10.1023/B:WIBI.0000023843.83692.3f

    Article  Google Scholar 

  55. Freedman ZB, Zak DR (2015) Atmospheric N deposition alters connectance, but not functional potential among saprotrophic bacterial communities. Mol Ecol 24:3170–3180. https://doi.org/10.1111/mec.13224

    Article  CAS  PubMed  Google Scholar 

  56. Chadha N, Prasad R, Varma A (2015) Plant promoting activities of fungal endophytes associated with tomato roots from central Himalaya, India and their interaction with Piriformospora indica. Int J Pharm Bio Sci 6:343–333

    Google Scholar 

  57. Firrincieli A, Otillar R, Salamov A, Schmutz J, Khan Z, Redman RS, Fleck ND, Lindquist E, Grigoriev IV, Doty SL (2015) Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1. Front Microbiol 6:978. https://doi.org/10.3389/fmicb.2015.00978

    Article  PubMed  PubMed Central  Google Scholar 

  58. Hernández M, Dumont MG, Yuan Q, Conrad R (2015) Different bacterial populations associated with the roots and rhizosphere of rice incorporate plant-derived carbon. Appl Environ Microbiol 81:2244–2253. https://doi.org/10.1128/AEM.03209-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Green LE, Porras-Alfaro A, Sinsabaugh RL (2008) Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. J Ecol 96:1076–1085. https://doi.org/10.1111/j.1365-2745.2008.01388.x

    Article  CAS  Google Scholar 

  60. Shabanamol S, Divya K, George TK, Rishad KS, Sreekumar TS, Jisha MS (2018) Characterization and in planta nitrogen fixation of plant growth promoting endophytic diazotrophic Lysinibacillus sphaericus isolated from rice (Oryza sativa). Physiol Mol Plant Pathol 102:46–54. https://doi.org/10.1016/j.pmpp.2017.11.003

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We appreciate Prof. Wenxue Wei (the Institute of Subtropical Agriculture, CAS) for the assistance with soil sampling and Dr. Jun Xiong (Fujian Agriculture and Forestry University) for the help with endophytic DNA extraction.

Funding

This work was supported by the National Natural Science Foundation of China (41525002, 41773079) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020303).

Author information

Authors and Affiliations

  1. Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, No. 1799 Jimei Road, Xiamen, 361021, China

    Xi-En Long & Huaiying Yao

  2. School of Geographic Sciences, Nantong University, No. 999 Tongjing Road, Nantong, 226007, China

    Xi-En Long

  3. Research Center for Environmental Ecology and Engineering, School of Environmental Ecology and Biological Engineering, Wuhan Institute of Technology, 206 Guanggu 1st Road, Wuhan, 430205, China

    Huaiying Yao

Authors
  1. Xi-En Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huaiying Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huaiying Yao.

Electronic supplementary material

ESM 1

(PDF 10070 kb)

ESM 2

(XLSX 71 kb)

ESM 3

(CSV 23 kb)

ESM 4

(XLSX 677 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Long, XE., Yao, H. Phosphorus Input Alters the Assembly of Rice (Oryza sativa L.) Root-Associated Communities. Microb Ecol 79, 357–366 (2020). https://doi.org/10.1007/s00248-019-01407-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01407-6

Keywords

Search

Navigation