Characterization and variation of the rhizosphere fungal community structure of cultivated tetraploid cotton

Autoři: Qinghua Qiao aff001;  Jingxia Zhang aff002;  Changle Ma aff001;  Furong Wang aff001;  Yu Chen aff002;  Chuanyun Zhang aff002;  Hui Zhang aff001;  Jun Zhang aff001
Působiště autorů: Key Laboratory of Plant Stress Research, College of Life Sciences, Shandong Normal University, Jinan, China aff001;  Key Laboratory of Cotton Breeding and Cultivation in Huang-Huai-Hai Plain, Ministry of Agriculture, Cotton Research Center of Shandong Academy of Agricultural Sciences, Jinan, China aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0207903


Rhizosphere fungal communities exert important influencing forces on plant growth and health. However, information on the dynamics of the rhizosphere fungal community structure of the worldwide economic crop cotton (Gossypium spp.) is limited. In the present study, next-generation sequencing of nuclear ribosomal internal transcribed spacer-1 (ITS1) was performed to characterize the rhizosphere fungal communities of G. hirsutum cv. TM-1 (upland cotton) and G. barbadense cv. Hai 7124 (island cotton). The plants were grown in field soil (FS) that had been continuously cropped with cotton and nutrient-rich soil (NS) that had not been cropped. The fungal species richness, diversity, and community composition were analyzed and compared among the soil resources, cotton genotypes, and developmental stages. We found that the fungal community structures were different between the rhizosphere and bulk soil and the difference were significantly varied between FS and NS. Our results suggested that cotton rhizosphere fungal community structure variation may have been primarily influenced by the interaction of cotton roots with different soil resources. We also found that the community composition of the cotton rhizosphere fungi varied significantly during different developmental stages. In addition, we observed fungi that was enriched or depleted at certain developmental stages and genotypes in FS and NS, and these insights can lay a foundation for deep research into the dynamics of pathogenic fungi and nutrient absorption of cotton roots. This research illustrates the characteristics of the cotton rhizosphere fungal communities and provides important information for understanding the potential influences of rhizosphere fungal communities on cotton growth and health.

Klíčová slova:

Agricultural soil science – Community structure – Cotton – Fungal structure – Fungi – Plant fungal pathogens – Rhizosphere – Seedlings


1. Perez-Jaramillo JE, Mendes R, Raaijmakers JM. Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant molecular biology. 2016;90(6):635–44. 26085172

2. Tkacz A, Cheema J, Chandra G, Grant A, Poole PS. Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. ISME J. 2015;9(11):2349–59. 25909975

3. Kazeeroni EA, Al-Sadi AM. 454-pyrosequencing reveals variable fungal diversity across farming systems. Front Plant Sci. 2016;7:314. 27014331

4. Zarraonaindia I, Owens SM, Weisenhorn P, West K, Hampton-Marcell J, Lax S, et al. The soil microbiome influences grapevine-associated microbiota. mBio. 2015;6(2):e02527–14. 25805735

5. Bulgarelli D, Garrido-Oter R, Münch Philipp C, Weiman A, Dröge J, Pan Y, et al. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell host & microbe. 2015;17(3):392–403. 25732064

6. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbe J, et al. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PloS one. 2013;8(10):e76382. 24146861

7. Wu Q-S, Zou Y-N, Huang Y-M. The arbuscular mycorrhizal fungus Diversispora spurca ameliorates effects of waterlogging on growth, root system architecture and antioxidant enzyme activities of citrus seedlings. Fungal Ecology. 2013;6(1):37–43.

8. Vd Gannes, Eudoxie G, Bekele I, Hickey WJ. Relations of microbiome characteristics to edaphic properties of tropical soils from Trinidad. Frontiers in microbiology. 2015;6:1045. 26483772

9. Xu Z, Yu G, Zhang X, Ge J, He N, Wang Q, et al. The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of changbai mountain. Appl Soil Ecol. 2015;86:19–29.

10. Eva O, Barbara G, Wolfgang W, Andrea W, Christian S, Yvonne S, et al. Microbial decomposition of 13C- labeled phytosiderophores in the rhizosphere of wheat: Mineralization dynamics and key microbial groups involved. Soil Biol Biochem. 2016;98:196–207.

11. Itoh K. Study of the ecology of pesticide-degrading microorganisms in soil and an assessment of pesticide effects on the ecosystem. J Pestic Sci. 2014;39(3):174–6.

12. Kotoky R, Rajkumari J, Pandey P. The rhizosphere microbiome: Significance in rhizoremediation of polyaromatic hydrocarbon contaminated soil. Journal of Environmental Management. 2018;217:858–70. 29660711

13. Dai P, Zong Z, Ma Q, Wang Y. Isolation, evaluation and identification of rhizosphere actinomycetes with potential application for biocontrol of Valsa mali. European Journal of Plant Pathology. 2018;153(1):1–12.

14. Trivedi P, Delgado-Baquerizo M, Trivedi C, Hu H, Anderson IC, Jeffries TC, et al. Microbial regulation of the soil carbon cycle: evidence from gene-enzyme relationships. The ISME journal. 2016;10(11):2593–604. 27168143

15. Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI. Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS microbiology ecology. 2016;92(7). 27130939

16. Cotta SR, Dias ACF, Seldin L, Andreote FD, Elsas JDv. The diversity and abundance of phytase genes (β-propeller phytases) in bacterial communities of the maize rhizosphere. Lett Appl Microbiol. 2016;62(3):264–8. 26661994

17. Kertesz MA, Mirleau P. The role of soil microbes in plant sulphur nutrition. J Exp Bot. 2004;55(404):1939. 15181108

18. Igiehon NO, Babalola OO. Rhizosphere Microbiome Modulators: Contributions of Nitrogen Fixing Bacteria towards Sustainable Agriculture. International Journal of Environmental Research & Public Health. 2018;15(4). 29570619

19. Ellouze W, Esmaeili Taheri A, Bainard LD, Yang C, Bazghaleh N, Navarro-Borrell A, et al. Soil Fungal Resources in Annual Cropping Systems and Their Potential for Management. BioMed Res Int. 2014;2014:15. 25247177

20. Wakelin SA, Warren RA, Harvey PR, Ryder MH. Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fert Soils. 2004;40(1):36–43.

21. Mittal V, Singh O, Nayyar H, Kaur J, Tewari R. Stimulatory effect of phosphate-solubilizing fungal strains (Aspergillus awamori and Penicillium citrinum) on the yield of chickpea (Cicer arietinum L. cv. GPF2). Soil Biol Biochem. 2008;40(3):718–27.

22. Xiao C, Chi R, He H, Qiu G, Wang D, Zhang W. Isolation of phosphate-solubilizing fungi from phosphate mines and their effect on wheat seedling growth. Appl Biochem Biotechnol. 2009;159(2):330–42. 19277482

23. Magdalena F, Silja EH, Marta B, Jedryczka M. Fungal biodiversity and their role in soil health. Front Microbiol. 2018;9:707. 29755421

24. Chapelle E, Mendes R, Bakker PA, Raaijmakers JM. Fungal invasion of the rhizosphere microbiome. ISME J. 2016;10(1):265–8. 26023875

25. Zhang Y, He J, Jia L-J, Yuan T-L, Zhang D, Guo Y, et al. Cellular tracking and gene profiling of fusarium graminearum during maize stalk rot disease development elucidates its strategies in confronting phosphorus limitation in the host apoplast. PLOS Pathog. 2016;12(3):e1005485. 26974960

26. Rebbeck J, Malone MA, Short D, Kasson MT, O’Neal ES, Davis DD. First report of verticillium wilt caused by Verticillium nonalfalfaeon tree-of-heaven (Ailanthus altissima) in Ohio. Plant Dis. 2013;97(7):999–1000. 30722582

27. Manjunatha SV, Naik MK, Mohamed FR, Goswami RS. Evaluation of bio-control agents for management of dry root rot of chickpea caused by Macrophomina phaseolina. Crop Protection. 2013;45(2):147–50.

28. Bacharis C, Gouziotis A, Kalogeropoulou P, Koutita O, Tzavella-Klonari K, Karaoglanidis GS. Characterization of Rhizoctonia spp. isolates associated with damping-off disease in cotton and tobacco seedlings in Greece. Plant Dis. 2010;94(11):1314–22. 30743646

29. Sanogo S, Zhang J. Resistance sources, resistance screening techniques and disease management for Fusarium wilt in cotton. Euphytica. 2015;207(2):255–71.

30. Laidou IA, Koulakiotu EK, Thanassoulopoulos CC. First report of stem canker caused by Alternaria alternata on cotton. Plant Dis. 2007;84(1):103.

31. Zhang W, Zhang H, Qi F, Jian G. Generation of transcriptome profiling and gene functional analysis in Gossypium hirsutum upon Verticillium dahliae infection. Biochem Bioph Res Co. 2016;473(4):879–85.

32. Knox O, Vadakattu G, Lardner R. Field evaluation of the effects of cotton variety and GM status on rhizosphere microbial diversity and function in Australian soils. Soil Res. 2014;52(2):203–215.

33. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488(7409):86–90. 22859206

34. Qiao Q, Wang F, Zhang J, Chen Y, Zhang C, Liu G, et al. The Variation in the Rhizosphere Microbiome of Cotton with Soil Type, Genotype and Developmental Stage. Sci Rep. 2017;7(1):3940. 28638057

35. Schloss PD. A high-throughput DNA sequence aligner for microbial ecology studies. PloS one. 2009;4(12):e8230. 20011594

36. Whalley WR, Riseley B, Leeds-Harrison PB, Bird NRA, Leech PK, Adderley WP. Structural differences between bulk and rhizosphere soil. Eur J Soil Sci. 2005;56(3):353–60.

37. Gould IJ, Quinton JN, Weigelt A, Deyn GBD, Bardgett RD. Plant diversity and root traits benefit physical properties key to soil function in grasslands. Ecol Lett. 2016;19(9):1140–39. 27459206

38. Odell RE, Dumlao MR, Samar D, Silk WK. Stage-dependent border cell and carbon flow from roots to rhizosphere. American journal of botany. 2008;95(4):441–6. 21632368

39. Bjørnlund L, Mørk S, Vestergård M, Rønn R. Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley. Biol Fert Soils 2006;43(1):1–11.

40. Stumpf L, Pauletto EA, Pinto LFS. Soil aggregation and root growth of perennial grasses in a constructed clay minesoil. Soil Till Res. 2016;161:71–8.

41. Zhu S, Vivanco JM, Manter DK. Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol. 2016;107:324–33.

42. Watson BS, Bedair MF, Urbanczyk-Wochniak E, Huhman DV, Yang DS, Allen SN, et al. Integrated metabolomics and transcriptomics reveal enhanced specialized metabolism in Medicago truncatula root border cells. Plant Physiol. 2015;167(4):1699–716. 25667316

43. Haichar FeZ, Santaella C, Heulin T, Achouak W. Root exudates mediated interactions belowground. Soil Biol Biochem. 2014;77:69–80.

44. Sasse J, Martinoia E, Northen T. Feed your friends: Do plant exudates shape the root microbiome?. Trends Plant Sci. 2018; 23(1):25–41. 29050989

45. Plancot B, Santaella C, Jaber R, Kiefer-Meyer MC, Follet-Gueye M-L, Leprince J, et al. Deciphering the responses of root border-like cells of Arabidopsis and flax to pathogen-derived elicitors. Plant Physiol. 2013;163(4):1584. 24130195

46. Curlango-Rivera G, Huskey DA, Mostafa A, Kessler JO, Xiong Z, Hawes MC. Intraspecies variation in cotton border cell production: rhizosphere microbiome implications. Am J Bot. 2013;100(9):1706–12. 23942085

47. Kawasaki A, Donn S, Ryan PR, Mathesius U, Devilla R, Jones A, et al. Microbiome and exudates of the root and rhizosphere of brachypodium distachyon, a model for wheat. PloS one. 2016;11(10):e0164533. 27727301

48. Chen Z, Tian Y, Zhang Y, Song BR, Li H, Chen Z. Effects of root organic exudates on rhizosphere microbes and nutrient removal in the constructed wetlands. Ecol Eng. 2016;92:243–50.

49. Bulgarelli D, Schlaeppi K, Spaepen S, Themaat EVLv, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol. 2013;64(1):807–38. 23373698

50. Edwardsa J, Johnsona C, Santos-Medellína C, Luriea E, Podishettyb NK, Bhatnagarc S, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Nat Acad Sci. 2015;112(8):E911–E20. 25605935

51. Xu L, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biol Biochem. 2012;46:26–32.

52. Bakker MG, Chaparro JM, Manter DK, Vivanco JM. Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant Soil. 2015;392(1–2):115–26.

53. Ling N, Kaiying D, Song Y, Wu Y, Zhao J, Raza W, et al. Variation of rhizosphere bacterial community in watermelon continuous mono-cropping soil by long-term application of a novel bioorganic fertilizer. Microbiol Res. 2014;169(7–8):570. 24263158

54. Gleń-Karolczyk K, Boligłowa E, Antonkiewicz J. Organic fertilization shapes the biodiversity of fungal communities associated with potato dry rot. Applied Soil Ecology. 2018.

55. Zhang W, Long X, Huo X, Chen Y, Lou K. 16S rRNA-Based PCR-DGGE Analysis of Actinomycete Communities in Fields with Continuous Cotton Cropping in Xinjiang, China. Microbial Ecol. 2013;66(2):385–93. 23299346

56. Vargas Gil S, Meriles J, Conforto C, Figoni G, Basanta M, Lovera E, et al. Field assessment of soil biological and chemical quality in response to crop management practices. World J Microbiol Biotech. 2009;25(3):439–48.

57. Peralta AL, Sun Y, Mcdaniel MD, Lennon JT. Crop rotational diversity increases disease suppressive capacity of soil microbiomes. Ecosphere. 2018;9(5):e02235.

58. Bai L, Cui J, Jie W, Cai B. Analysis of the community compositions of rhizosphere fungi in soybeans continuous cropping fields. Microbiol Res. 2015;180(Supplement C):49–56. 26505311

59. Fu Q, Liu C, Ding N, Lin Y, Guo B, Luo J, et al. Soil microbial communities and enzyme activities in a reclaimed coastal soil chronosequence under rice–barley cropping. J Soil Sediment. 2012;12(7):1134–44.

60. Baudoin E, Benizri E, Guckert A. Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. ApplSoil Ecol. 2002;19(2):135–45.

61. Okubo T, Tokida T, Ikeda S, Bao Z, Tago K, Hayatsu M, et al. Effects of elevated carbon dioxide, elevated temperature, and rice growth stage on the community structure of rice root-associated bacteria. Microbes Environ. 2014;29(2):184–90. 24882221

62. İnceoğlu Ö, Salles JF, Overbeek Lv, Elsas JDv. Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl Environ Microbiol. 2010;76(11):3675–584. 20363788

63. Li X, Rui J, Mao Y, Yannarell A, Mackie R. Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem. 2014;68:392–401.

64. Breidenbach B, Pump J, Dumont MG. Microbial community structure in the rhizosphere of rice plants. Front Microbiol. 2016;6:1537. 26793175

65. Schlemper TR, Mfa L, Lucheta AR, Shimels M, Bouwmeester HJ, van Veen JA, et al. Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS microbiology ecology. 2017;93(8):1–11. 28830071

66. Schmidt CS, Alavi M, Cardinale M, Müller H, Berg G. Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere. Biology and Fertility of Soils. 2012;48(8):947–60.

67. Elsharkawya MM, Shivannab MB, Manchanahally, Meerab S, Hyakumachic M. Mechanism of induced systemic resistance against anthracnose disease in cucumber by plant growth-promoting fungi. Acta Agriculturae Scandinavica, Section B—Soil & Plant Science. 2015;65(4):287–99.

68. Zhang J, Liu Y-X, Zhang N, Hu B, Jin T, Xu H, et al. Nrt1.1b Is Associated with Root Microbiota Composition and Nitrogen Use in Field-Grown Rice. Nature Biotechnology. 2019;37:676–84. 31036930

69. Wang Z, Li T, Wen X, Liu Y, Han J, Liao Y, et al. Fungal Communities in Rhizosphere Soil under Conservation Tillage Shift in Response to Plant Growth. Front Microbiol. 2017;8:1301. 28744278

70. Poli A, Lazzari A, Prigione V, Voyron S, Spadaro D, Varese GC. Influence of plant genotype on the cultivable fungi associated to tomato rhizosphere and roots in different soils. Fungal Biol. 2016;120(6–7):862–72. 27268246

71. Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3(4):470–80. 29556109

72. A C-L, A D, A O, M E-U, T K. Rosmarinic acid is a homoserine lactone mimic produced by plants that activates a bacterial quorum-sensing regulator. Science Signaling. 2016;9(409):ra1. 26732761

73. Kudjordjie EN, Sapkota R, Steffensen SK, Fomsgaard IS, Nicolaisen M. Maize synthesized benzoxazinoids affect the host associated microbiome. Microbiome. 2019;7(59). 30975184

74. Jogaiah S, Abdelrahman M, Phan Tran L-S, Ito Shin-ichi. Characterization of rhizosphere fungi that mediate resistance in tomato against bacterial wilt disease. Journal of Experimental Botany. 2013;64(12):3829–42. 23956415

75. Morales A, Marysol A, Valenzuela E, Rubio R, Borie F. Effect of inoculation with Penicillium albidum, a phosphate-solubilizing fungus, on the growth of Trifolium pratense cropped in a volcanic soil. J Basic Microb. 2007;47(3):275–80. 17518421

76. Gong M, Du P, Liu X, Zhu C. Transformation of Inorganic P Fractions of Soil and Plant Growth Promotion by Phosphate-solubilizing Ability of Penicillium oxalicum I1. J Microbiol. 2014;52(12):1012–9. 25363630

77. Al-Hosni K, Shahzad R, Latif Khan A, Muhammad Imran Q, Al Harrasi A, Al Rawahi A, et al. Preussia sp. BSL-10 producing nitric oxide, gibberellins, and indole acetic acid and improving rice plant growth. Journal of Plant Interactions. 2018;13(1):112–8.

78. JN N, JK P, DG W. Development of Gibberella Ear Rot on Processing Sweet Corn Hybrids Over an Extended Period of Harvest. Plant Disease. 2007;91(2):171–5. 30781000

Článek vyšel v časopise


2019 Číslo 10