Advertisement

Microenvironment and microbial community in the rhizosphere of dioecious Populus cathayana at Chaka Salt Lake

  • Na Wu
  • Zhen Li
  • Fei Wu
  • Ming TangEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article

Abstract

Purpose

Sex effects may cause significant changes in rhizosphere microbial community composition and soil properties. Although dioecious plants are widespread, little is known about rhizosphere microenvironmental differences in response to dioecious plants.

Materials and methods

This study characterized microbial species by next-generation sequencing and evaluation of soil properties in the rhizosphere of male and female Populus cathayana plants located in non-saline area (control site), salt lakeside (low salt), salt mountain (middle salt), and salt factory (high salt) areas.

Results and discussion

A total of 5 phyla, 18 classes, 57 orders, 108 families, and 211 genera of fungi were observed in the rhizosphere of P. cathayana, while 18 phyla, 35 classes, 69 orders, 149 families, and 329 genera of bacteria were observed in the rhizosphere of P. cathayana. With increasing salinization, the microbial community diversity in the rhizosphere of P. cathayana first increased and then decreased, especially in the fungal community. Site and sex had significant effects on microbial communities and caused adjustments in microbial community structure. Redundancy analysis (RDA) showed that available K, ammonium nitrogen (NH4-N), and nitrate nitrogen (NO3-N) as well as Na+ and Cl contents and the electrical conductivity (EC) were the main factors affecting the microbial community in the rhizosphere of P. cathayana in the Chaka Salt Lake ecosystem.

Conclusions

This is the first study focusing on microbial communities and soil properties in the rhizosphere of male and female P. cathayana plants with different degrees of salinity. In addition, potential differences in the preferences of the microbial communities between the two sexes exist.

Keywords

Dioecious Microbial community Microenvironment Populus cathayana Salinity 

Notes

Authors’ contribution

N Wu and Z Li have contributed equally to this work. N Wu and Z Li designed the experiments, collected and analyzed the experimental data, and prepared the first draft under supervision of Prof. M. Tang. F Wu modified the manuscript. All authors contributed substantially to revising the manuscript.

Funding information

This study was supported by the National Key Research and Development Program of China (2018YFD0600203) and National Natural Science Foundation of China (41671268)‍.

Supplementary material

11368_2019_2263_MOESM1_ESM.docx (1.4 mb)
ESM 1 (DOCX 1.44 mb)
11368_2019_2263_MOESM2_ESM.docx (55 kb)
ESM 2 (DOCX 55.1 kb)

References

  1. Ban YH, Tang M, Chen H, Xu ZY, Zhang HH, Yang YR (2012) The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One 7:e47968.  https://doi.org/10.1371/journal.pone.0047968 CrossRefGoogle Scholar
  2. Banik A, Pandya P, Patel B, Rathod C, Danger M (2018) Characterization of halotolerant, pigmented, plant growth promoting bacteria of groundnut rhizosphere and its in-vitro evaluation of plant-microbe protocooperation to withstand salinity and metal stress. Sci Total Environ 630:231–242CrossRefGoogle Scholar
  3. Barrett SCH, Hough J (2013) Sexual dimorphism in flowering plants. J Exp Bot 64:67–82CrossRefGoogle Scholar
  4. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  5. Chen S, Li J, Wang S, Hüttermann A, Altman A (2001) Salt, nutrient uptake and transport, and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees Struct Funct 15:186–194CrossRefGoogle Scholar
  6. Chen FG, Chen LH, Zhao HX, Korpelainen H, Li CY (2010) Sex-specific responses and tolerance of Populus cathayana to salinity. Physiol Plantarum 140:163–173CrossRefGoogle Scholar
  7. Chen FS, Yavitt J, Hu XF (2014) Phosphorus enrichment helps increase soil carbon mineralization in vegetation along an urban-to-rural gradient, Nanchang, China. Appl Soil Ecol 75:181–188CrossRefGoogle Scholar
  8. Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, Charron P, St-Onge C et al (2018) High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220:1161–1171CrossRefGoogle Scholar
  9. Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, London, pp 278–309CrossRefGoogle Scholar
  10. Estavillo JM, Rodriguez M, Lacuesta M, GonzalezMurua C (1997) Effects of cattle slurry and mineral N fertilizer application on various components of the nitrogen balance of mown grassland. Plant Soil 188:49–58CrossRefGoogle Scholar
  11. Feng Y, Schubert S, Mengel K (1996) Soil pH increase due to biological decarboxylation of organic anions. Soil Biol Biochem 28:617–624CrossRefGoogle Scholar
  12. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefGoogle Scholar
  13. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal endo-gone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244CrossRefGoogle Scholar
  14. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  15. Guwy AJ, Martin SR, Hawkes FR, Hawkes DL (1999) Catalase activity measurements in suspended aerobic biomass and soil samples. Enzyme Microb Technol 25:669–676CrossRefGoogle Scholar
  16. Hacquard S, Schadt CW (2014) Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol 205:1424–1430CrossRefGoogle Scholar
  17. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  18. Joergensen RG, Wichern F (2018) Alive and kicking: why dormant soil microorganisms matter. Soil Biol Biochem 116:419–430CrossRefGoogle Scholar
  19. Kandeler E, Eder G (1993) Effect of cattle slurry in grassland on microbial biomass and on activities of various enzymes. Biol Fertil Soils 16:249–254CrossRefGoogle Scholar
  20. Lee EA, Weiss SL, Lam M, Torres R, Diamond J (1998) A method for assaying intestinal brush-border sucrase in an intact intestinal preparation. PNAS 95:2111–2116CrossRefGoogle Scholar
  21. Li M, Wang M, Wang Q (2006) Development and performance test of a portable soil EC detector. Appl Eng Agric 22:301–307CrossRefGoogle Scholar
  22. Li Z, Wu N, Liu T, Chen H, Tang M (2015) Effect of arbuscular mycorrhizal inoculation on water status and photosynthesis of Populus cathayana males and females under water stress. Physiol Plantarum 155:192–204Google Scholar
  23. 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 118:103–114CrossRefGoogle Scholar
  24. Maciá-Vicente JG, Ferraro V, Burruano S, Lopez-Llorca LV (2012) Fungal assemblages associated with roots of halophytic and non-halophytic plant species vary differentially along a salinity gradient. Environ Microbiol 64:668–679Google Scholar
  25. Malherbe S, Marais D (2015) Nematode community profiling as soil biology monitoring tool in support of sustainable tomato production: a case study from South Africa. Appl Soil Ecol 93:19–27CrossRefGoogle Scholar
  26. Mandyam KG, Jumpponen A (2015) Mutualism-parasitism paradigm synthesized from results of root-endophyte models. Front Microbiol 5:776.  https://doi.org/10.3389/fmicb.2014.00776
  27. Mosier SL, Kane ES, Richter DL, Lilleskov EA, Jurgensen MF, Burton AJ, Resh SC (2017) Interactive effects of climate change and fungal communities on wood-derived carbon in forest soils. Soil Biol Biochem 115:297–309CrossRefGoogle Scholar
  28. Munné-Bosch S (2015) Sex ratios in dioecious plants in the framework of global change. Environ Exp Bot 109:99–102CrossRefGoogle Scholar
  29. Muyzer G, DeWaal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700Google Scholar
  30. Paudel S, Benavides JC, MacDonald B, Longcore T, Wilson GWT, Loss SR (2017) Determinants of native and non-native plant community structure on an oceanic island. Ecosphere 8(9):e01927.  https://doi.org/10.1002/ecs2.1927
  31. Peng Y, Zhu Y, Mao Y, Wang S, Su W, Tang Z (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55:939–949CrossRefGoogle Scholar
  32. Perdok UD, Kroesbergen B, Hilhorst MA (1996) Influence of gravimetric water content and bulk density on the dielectric properties of soil. Eur J Soil Sci 47:367–371CrossRefGoogle Scholar
  33. Phillips J, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55:158–161CrossRefGoogle Scholar
  34. Pozo C, Martineztoledo MV, Salmeron V, Rodelas B, Gonzalezlopez J (1995) Effects of chlorpyrifos on soil microbial activity. Environ Toxicol Chem 14:187–192CrossRefGoogle Scholar
  35. Price JR, Ledford SH, Ryan MO, Toran L, Sales CM (2018) Wastewater treatment plant effluent introduces recoverable shifts in microbial community composition in receiving streams. Sci Total Environ 613:1104–1116CrossRefGoogle Scholar
  36. Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606CrossRefGoogle Scholar
  37. Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363CrossRefGoogle Scholar
  38. Rodriguez RJ, Redman RS (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114CrossRefGoogle Scholar
  39. Salazar-Cerezo S, Martinez-Montiel N, Cruz-Lopez MD, Martinez-Contreras RD (2018) Fungal diversity and community composition of culturable fungi in Stanhopea trigrina Cast Gibberellin producers. Front Microbiol 9:612.  https://doi.org/10.3389/fmicb.2018.00612
  40. Sanchez-Bel P, Sanmartin N, Pastor V, Mateu D, Cerezo M, Vidal-Albalat A, Pastor-Fernandez J, Pozo MJ et al (2018) Mycorrhizal tomato plants from fine tunes the growth-defence balance upon N depleted root environments. Plant Cell Environ 41:406–420CrossRefGoogle Scholar
  41. Santangelo JS, Kotanen PM (2016) Nonsystemic fungal endophytes increase survival but reduce tolerance to simulated herbivory in subarctic Festuca rubra. Ecosphere 7(5):e01260.  https://doi.org/10.1002/ecs2.1260
  42. Seleiman MF, Kheir AMS (2018) Saline soil properties, quality and productivity of wheat grown with bagasse ash and thiourea in different climatic zones. Chemosphere 193:538–546CrossRefGoogle Scholar
  43. Shao TY, Zhao JJ, Zhu TS, Chen MX, Wu YW, Long XH et al (2018) Relationship between rhizosphere soil properties and blossom-end rot of tomatoes in coastal saline-alkali land. Appl Soil Ecol 127:96–101CrossRefGoogle Scholar
  44. Soares MA, Li HY, Kowalski KP, Bergen M, Torres MS, White JF (2016) Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biol Invasions 18:2689–2702CrossRefGoogle Scholar
  45. Song YY, Song CC, Ren JS, Tan WW, Jin SF, Jiang L (2018) Influence of nitrogen additions on litter decomposition, nutrient dynamics, and enzymatic activity of two plant species in a peatland in Northwest China. Sci Total Environ 625:640–646CrossRefGoogle Scholar
  46. Stahl M, Widney S, Craft C (2018) Tidal freshwater forests: sentinels for climate change. Ecol Eng 116:104–109CrossRefGoogle Scholar
  47. Sun H, Santalahti M, Pumpanen J, Köster K, Berninger F, Raffaello T, Jumpponen A, Asiegbu F et al (2015) Fungal community shifts in structure and function across a boreal forest fire chronosequence. Appl Environ Microbiol 81:7869–7880CrossRefGoogle Scholar
  48. Tu Q, Yu H, He Z, Deng Y, Wu L, Nostrand JD, Zhou A, Voordeckers J et al (2014) GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol Ecol Resour 14:914–928Google Scholar
  49. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefGoogle Scholar
  50. Uma E, Sathiyadash K, Loganathan J, Muthukumar T (2012) Tree species as hosts for arbuscular mycorrhizal and dark septate endophyte fungi. J Forest Res 23:641–649CrossRefGoogle Scholar
  51. Vergara C, Araujo KEC, Urquiaga S, Schultz N, Balieiro FD, Medeiros PS, Santos LA, Xavier GR, et al (2017) Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material. Front Microbiol 8:2437.  https://doi.org/10.3389/fmicb.2017.02437
  52. Vogt JC, Abed R, Albach DC, Palinska KA (2018) Bacterial and archaeal diversity in Hypersaline Cyanobacterial mats along a transect in the intertidal flats of the sultanate of Oman. Microb Ecol 75:331–347CrossRefGoogle Scholar
  53. Wang M, Li EQ, Liu C, Jousset A, Salles JF (2017) Functionality of root-associated bacteria along a salt marsh primary succession. Front Microbiol 8:2102Google Scholar
  54. Watson GK, Cain RB (1975) Microbial metabolism of the pyridine ring. Metabolic pathways of pyridine biodegradation by soil bacteria. Biochem J 146:157–172CrossRefGoogle Scholar
  55. White T (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. PCR protocols: a guide to methods and applicationsGoogle Scholar
  56. Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H (2010) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561CrossRefGoogle Scholar
  57. Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107CrossRefGoogle Scholar
  58. Wu N, Li Z, Liu H, Tang M (2015) Influence of arbuscular mycorrhiza on photosynthesis and water status of Populus cathayana Rehder males and females under salt stress. Acta Physiol Plant 37:183CrossRefGoogle Scholar
  59. Wu N, Li Z, Wu F, Tang M (2016) Comparative photochemistry activity and antioxidant responses in male and female Populus cathayana cuttings inoculated with arbuscular mycorrhizal fungi under salt stress. Sci Rep 6:37663.  https://doi.org/10.1038/srep37663
  60. Yamamoto M, Nakata H, Kumchantuek T, Adhapanyawanich K, Iseki S (2018) Distinct hormonal regulation of two types of sexual dimorphism in submandibular gland of mice. Cell Tissue Res 371:261–272CrossRefGoogle Scholar
  61. Yan N, Marschner P (2013) Response of soil respiration and microbial biomass to changing EC in saline soils. Soil Biol Biochem 65:322–328.  https://doi.org/10.1016/j.soilbio.2013.06.008
  62. Yao H, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environ Microbiol 15(9):2545–2556CrossRefGoogle Scholar
  63. Yao Z, Xing J, Gu H, Wang H, Wu J, Xu J, Brookes PC (2016) Development of microbial community structure in vegetable-growing soils from open-field to plastic-greenhouse cultivation based on the PLFA analysis. J Soils Sediments 16:2041–2049CrossRefGoogle Scholar
  64. Zhang Y, Wang LJ, Yuan YG, Xu J, Tu C, Fisk C et al (2018) Irrigation and weed control alter soil microbiology and nutrient availability in North Carolina Sandhill peach orchards. Sci Total Environ 615:517–525CrossRefGoogle Scholar
  65. Zhao HX, Li YP, Zhang XL, Korpelainen H, Li CY (2012) Sex-related and stage-dependent source-to-sink transition in Populus cathayana grown at elevated CO2 and elevated temperature. Tree Physiol 32:1325–1338CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources (South China Agricultural University), Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape ArchitectureSouth China Agricultural UniversityGuangzhouChina
  2. 2.School of Life SciencesShanxi Datong UniversityDatongChina
  3. 3.2011 Collaborative Innovation Center of Jiangxi Typical Trees Cultivation and Utilization, College of ForestryJiangxi Agricultural UniversityNanchangChina

Personalised recommendations