Plant Growth Regulation

, Volume 87, Issue 2, pp 257–266 | Cite as

Composition and diversity of endophytic bacterial community in seeds of super hybrid rice ‘Shenliangyou 5814’ (Oryza sativa L.) and its parental lines

  • Yang LiuEmail author
  • Pengpeng Xu
  • Fuzhen Yang
  • Miao Li
  • Hai Yan
  • Ni Li
  • Xiaoxia ZhangEmail author
  • Weiping WangEmail author
Original paper


Super hybrid rice is one of the important research achievements in the field of rice super-high yield breeding in China. Compared with general high-yield rice, the yield potential of super hybrid rice is relatively high, and the average yields per hectare can exceed 10.5 t. This study aimed to study the endophytic bacterial community among a super hybrid rice combination and its parental lines and to reveal the potential relationship and association of endophytic bacteria between rice genotypes and their genetic relevance. In this research, through high-throughput sequencing based on Illumina Hiseq 2500 platform, the seeds of super hybrid rice variety ‘Shenliangyou 5814’ (sample C) and its parental lines ‘Y58S’ (sample M) and ‘C4114’ (sample F) independently cultivated by China were used as plant materials to study their endophytic bacterial structure and diversity. The number of OTUs for sample M, F and C was 327, 288 and 283 respectively, and among them 218 endophytic OTUs coexisted in the 3 samples. Pantoea (18.6–31.1%) was the first dominant groups shared in all three samples, and other dominant shared groups belonged to Methylobacterium (4.48%~17.65%), Sphingomonas (4.0%~11.4%), Rhizobium (5.69–8.78%), Microbacterium (3.85%~9.41%) and Pseudomonas (4.13%~5.68%). Although Principal Coordinates Analysis (PCoA) and Non-metric Multidimensional Scaling (NMDS) analysis showed that there were obvious differences in endophytic bacterial community composition and structure among the 3 samples, the dominant endophytic bacterial genus sample C and its parental lines remained consistency. This study would provide scientific clues for the future research on the vertical transmission of endophytes between rice generations.


Super hybrid rice Shenliangyou 5814 Endophytic bacteria Diversity Seed 



This work was supported by the Fundamental Research Funds for the Central Universities (No. FRF-TP-18-012A1) and the Open Research Fund of State Key Laboratory of Hybrid Rice (Hunan Hybrid Rice Research Center) (No. 2017KF04). We also thank Dr. Zhengqiu Cai at Seres Therapeutics (USA) for assistance with English language and grammatical editing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Research involving human and animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10725_2018_467_MOESM1_ESM.ppt (486 kb)
Supplementary material 1 (PPT 485 KB)
10725_2018_467_MOESM2_ESM.doc (27 kb)
Supplementary material 2 (DOC 27 KB)


  1. Antunes JEL, Lyra MCCP, Ollero FJ, Freitas ADS, Oliveira LMS, Araújo ASF, Figueiredo MVB (2017) Diversity of plant growth-promoting bacteria associated with sugarcane. Genet Mol Res. Google Scholar
  2. Banik A, Mukhopadhaya SK, Dangar TK (2016) Characterization of N2-fixing plant growth promoting endophytic and epiphytic bacterial community of Indian cultivated and wild rice (Oryza spp.) genotypes. Planta 243(3):799–812CrossRefGoogle Scholar
  3. Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8(2):e56329CrossRefGoogle Scholar
  4. Buyer JS, Roberts DP, Russek-Cohen E (1999) Microbial community structure and function in the spermosphere as affected by soil and seed type. Can J Microbiol 45(2):138–144CrossRefGoogle Scholar
  5. Campestre MP, Castagno LN, Estrella MJ, Ruiz OA (2016) Lotus japonicus plants of the Gifu B-129 ecotype subjected to alkaline stress improve their Fe(2+) bio-availability through inoculation with Pantoea eucalypti M91. J Plant Physiol 192:47–55CrossRefGoogle Scholar
  6. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345CrossRefGoogle Scholar
  7. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11(4):265–270Google Scholar
  8. Chaudhry V, Baindara P, Pal VK, Chawla N, Patil PB, Korpole S (2016) Methylobacterium indicum sp. nov., a facultative methylotrophic bacterium isolated from rice seed. Syst Appl Microbiol 39(1):25–32CrossRefGoogle Scholar
  9. Cheng SH (2007) Innovation and development of rice breeding for super high yield in China (in Chinese). J Shenyang Agric Univ 38(5):647–651Google Scholar
  10. Durand A, Maillard F, Alvarez-Lopez V, Guinchard S, Bertheau C, Valot B, Blaudez D, Chalot M (2017) Bacterial diversity associated with poplar trees grown on a Hg-contaminated site: community characterization and isolation of Hg-resistant plant growth-promoting bacteria. Sci Total Environ 622–623:1165–1177Google Scholar
  11. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998CrossRefGoogle Scholar
  12. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200CrossRefGoogle Scholar
  13. Feng YJ, Shen DL, Dong XZ, Song W (2003) In vitro symplasmata formation in the rice diazotrophic endophyte Pantoea applomerans YS19. Plant Soil 255:435–444CrossRefGoogle Scholar
  14. Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287(1):8–14CrossRefGoogle Scholar
  15. Gitaitis R, Walcott R (2007) The epidemiology and management of seedborne bacterial diseases. Annu Rev Phytopathol 45:371–397CrossRefGoogle Scholar
  16. Grum M, Camloh M, Rudolph K, Ravnikar M (1998) Elimination of bean seed-borne bacteria by thermotherapy and meristem culture. Plant Cell Tissue Org Cult 52:79–82CrossRefGoogle Scholar
  17. Guan KL (2009) Seed physiological ecology (in Chinese). China Agriculture Press, BeijingGoogle Scholar
  18. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471CrossRefGoogle Scholar
  19. Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7(2):e30438CrossRefGoogle Scholar
  20. Huang Y, Kuang Z, Wang W, Cao L (2016) Exploring potential bacterial and fungal biocontrol agents transmitted from seeds to sprouts of wheat. Biol Control 98:27–33CrossRefGoogle Scholar
  21. Ji HT, Feng YH, He TB, Li Y, Wu B, Wang XY (2013) Dynamic characteristics of matter population in two super hybrid rice cultivars (in Chinese). Acta Agron Sin 39(12):2238–2246CrossRefGoogle Scholar
  22. Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169(1):83–98CrossRefGoogle Scholar
  23. Jiang XY, Gao JS, Xu FH, Cao YH, Tang X, Zhang XX (2013) Diversity of endophytic bacteria in rice seeds and their secretion of indole acetic acid (in Chinese). Acta Microbiol Sin 53:269–275Google Scholar
  24. Kloepper JW, Beauchamp CJ (1992) A review of issues related to measuring colonization of plant roots by bacteria. Can J Microbiol 38:1219–1232CrossRefGoogle Scholar
  25. Lamit LJ, Lau MK, Sthultz CM, Wooley SC, Whitham TG, Gehring CA (2014) Tree genotype and genetically based growth traits structure twig endophyte communities. Am J Bot 101:467–478CrossRefGoogle Scholar
  26. Li GC, Zhang SY, Xiao W, Long ZY, Zhang NM (2015) Research progress on endophytes in rice (in Chinese). Chin Agric Sci Bull 31(12):157–162Google Scholar
  27. Liu L, Liu Y, Song W (2009) Indigenous bacterial community diversity in hybrid rice (Oryza sativa L.) seed (in Chinese). Biotechnol Bull 1:95–111Google Scholar
  28. Liu Y, Zuo S, Xu LW, Zou YY, Song W (2011) Diversity of endophytic bacterial communities in seeds of hybrid maize (Zea mays L., Nongda108) and their parental lines (in Chinese). Sci Agric Sin 44(23):4763–4771Google Scholar
  29. Liu Y, Zuo S, Xu LW, Zou YY, Song W (2012a) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012CrossRefGoogle Scholar
  30. Liu Y, Zuo S, Zou YY, Wang JH, Song W (2012b) Investigation on diversity and population succession dynamics of indigenous bacteria of the maize spermosphere. World J Microbiol Biotechnol 28:391–396CrossRefGoogle Scholar
  31. Liu Y, Zuo S, Zou YY, Wang JH, Song W (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol 63:71–79CrossRefGoogle Scholar
  32. Liu Y, Yao S, Xu PP, Cao YH, Li JX, Wang JM, Tan WQ, Cheng C (2014) Composition and diversity of endophytic bacterial communities in noni (Morinda citrifolia L.) seeds. Int J Agric Policy Res 2(3):98–104Google Scholar
  33. Liu Y, Wang RH, Li YH, Cao YH, Chen CY, Qiu CZ, Bai FR, Xu TJ, Zhang X, Dai WK, Zhao JR, Cheng C (2017a) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of hybrid maize planted in China. Plant Growth Regul 81:317–324CrossRefGoogle Scholar
  34. Liu Y, Bai FR, Li N, Wang WP, Cheng C (2017b) Identification of endophytic bacterial strain RSE1 from seeds of super hybrid rice Shenliangyou 5814 (Oryza sativa L.,) and evaluation of its antagonistic activity. Plant Growth Regul 82:403–408CrossRefGoogle Scholar
  35. López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33(6):322–327CrossRefGoogle Scholar
  36. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963CrossRefGoogle Scholar
  37. Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23(2):109–117CrossRefGoogle Scholar
  38. Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 21:86–100CrossRefGoogle Scholar
  39. Mantica P, Tala T, Ferreira JS, Peeters AG, Salmi A, Strintzi D, Weiland J, Brix M, Giroud C, Corrigan G, Zastrow KD, Naulin V, Tardini G (2010) Perturbative studies of toroidal momentum transport using neutral beam injection modulation in the Joint European Torus: experimental results, analysis methodology, and first principles modeling. Phys Plasmas 17(9):112–134CrossRefGoogle Scholar
  40. Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, Braca T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytorem 11:251–267CrossRefGoogle Scholar
  41. Megías E, Reis Junior FB, Ribeiro RA, Megías M, Ollero FJ, Hungria M (2017) Genome sequence of Pantoea sp. strain 1.19, isolated from rice rhizosphere, with the capacity to promote growth of legumes and nonlegumes. Genome Announc 5(30):e00707–e00717CrossRefGoogle Scholar
  42. Mora Y, Díaz R, Vargas-Lagunas C, Peralta H, Guerrero G, Aguilar A, Encarnación S, Girard L, Mora J (2014) Nitrogen-fixing rhizobial strains isolated from common bean seeds: phylogeny, physiology, and genome analysis. Appl Environ Microbiol 80(18):5644–5654CrossRefGoogle Scholar
  43. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309CrossRefGoogle Scholar
  44. O’Keeffe J (2004) Measuring Biological Diversity. Afr J Aquat Sci 29(2):285–286CrossRefGoogle Scholar
  45. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124CrossRefGoogle Scholar
  46. Qin Y, Pan X, Yuan Z (2016) Seed endophytic microbiota in a coastal plant and phytobeneficial properties of the fungus Cladosporium cladosporioides. Fungal Ecol 24:53–60CrossRefGoogle Scholar
  47. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596CrossRefGoogle Scholar
  48. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Roehr JT, Dieterich C, Reinert K (2017) Flexbar 3.0-SIMD and multicore parallelization. Bioinformatics 33(18):2941–2942CrossRefGoogle Scholar
  50. Sánchez-López AS, Pintelon I, Stevens V, Imperato V, Timmermans JP, González-Chávez C, Carrillo-González R, Van Hamme J, Vangronsveld J, Thijs S (2018) Seed endophyte microbiome of Crotalaria pumila unpeeled: identification of plant-beneficial methylobacteria. Int J Mol Sci 19(1):291CrossRefGoogle Scholar
  51. Sasaki K, Ikeda S, Ohkubo T, Kisara C, Sato T, Minamisawa K (2013) Effects of plant genotype and nitrogen level on bacterial communities in rice shoots and roots. Microbes Environ 28:391–395CrossRefGoogle Scholar
  52. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  53. Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39(1):23–32CrossRefGoogle Scholar
  54. Sobolev VS, Orner VA, Arias RS (2013) Distribution of bacterial endophytes in peanut seeds obtained from axenic and control plant material under field conditions. Plant Soil 371:367–376CrossRefGoogle Scholar
  55. Tavares MJ, Nascimento FX, Glick BR, Rossi MJ (2018) The expression of an exogenous ACC deaminase by the endophyte Serratia grimesii BXF1 promotes the early nodulation and growth of common bean. Lett Appl Microbiol 66(3):252–259CrossRefGoogle Scholar
  56. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50CrossRefGoogle Scholar
  57. Truyens S, Beckers B, Thijs S, Weyens N, Cuypers A, Vangronsveld J (2016) Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana. Plant Biol 18(3):376–381CrossRefGoogle Scholar
  58. Van Overbeek L, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbl Ecol 64:283–296CrossRefGoogle Scholar
  59. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206CrossRefGoogle Scholar
  60. Verma SK, White JF (2018) Indigenous endophytic seed bacteria promote seedling development and defend against fungal disease in browntop millet (Urochloa ramosa L.). J Appl Microbiol 124(3):764–778CrossRefGoogle Scholar
  61. Wang ZW, Ji YL, Chen YG (2015) Studies and biological significances of plant endophytes (in Chinese). Microbiol China 42(2):349–363Google Scholar
  62. Yim W, Seshadri S, Kim K, Lee G, Sa T (2013) Ethylene emission and PR protein synthesis in ACC deaminase producing Methylobacterium spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with Ralstonia solanacearum under greenhouse conditions. Plant Physiol Biochem 67:95–104CrossRefGoogle Scholar
  63. Zhang L, Birch RG (1997) The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane. Proc Natl Acad Sci USA 94:9984–9989CrossRefGoogle Scholar
  64. Zhang J, Zhang CW, Yang J, Zhang RJ, Gao JS, Zhao X, Zhao JJ, Zhao DF, Zhang XX (2018) Insights into endophytic bacterial community structures of seeds among various Oryza sativa L. rice genotypes. J Plant Growth Regul. Google Scholar
  65. Zou YY, Liu L, Liu Y, Zhao L, Deng QY, Wu J, Zhuang W, Song W (2012) Diversity of indigenous bacterial communities in Oryza sativa seeds of different varieties (in Chinese). Chin J Plant Ecol 36:880–890CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of Chemistry and Biological EngineeringUniversity of Science and Technology BeijingBeijingChina
  2. 2.National Key Laboratory of Hybrid RiceHunan Hybrid Rice Research CenterChangshaChina
  3. 3.Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingChina
  4. 4.Nanjing Puwikon, Co., LtdNanjingChina

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