Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

The effect of Glomus intraradices on the physiological properties of Panax ginseng and on rhizospheric microbial diversity

  • Tian, Lei (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Shi, Shaohua (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Ma, Lina (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Zhou, Xue (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Luo, Shasha (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Zhang, Jianfeng (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) ;
  • Lu, Baohui (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Tian, Chunjie (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
  • Received : 2017.02.11
  • Accepted : 2017.08.14
  • Published : 2019.01.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Glomus intraradices is a species of arbuscular mycorrhizal fungi that, as an obligate endomycorrhiza, can form mutually beneficial associations with plants. Panax ginseng is a popular traditional Chinese medicine; however, problems associated with ginseng planting, such as pesticide residues, reduce the ginseng quality. Methods: In this experiment, we studied the effect of inoculating G. intraradices on several physiological properties and microbial communities of ginseng. UV-Visible Spectrum method was used to detect physical properties. Denaturing gradient gel electrophoresis method was used to analyze microbial communities. Results: The results indicated that inoculation with G. intraradices can improve the colonization rate of lateral ginseng roots, increase the levels of monomeric and total ginsenosides, and improve root activity as well as polyphenol oxidase and catalase activities. We also studied the bacterial and fungal communities in ginseng rhizospheric soil. In our study, G. intraradices inoculation improved the abundance and Shannon diversity of bacteria, whereas fungi showed a reciprocal effect. Furthermore, we found that G. intraradices inoculation might increase some beneficial bacterial species and decreased pathogenic fungi in rhizospheric soil of ginseng. Conclusion: Our results showed that G. intraradices can benefit ginseng planting which may have some instructive and practical significance for planting ginseng in farmland.

Keywords

References

  1. Li S, Li J, Yang XL, Cheng Z, Zhang WJ. Genetic diversity and differentiation of cultivated ginseng ( Panax ginseng C. A. Meyer) populations in North-east China revealed by inter-simple sequence repeat (ISSR) markers. Genet Resour Crop Evo 2011;58:815-24. https://doi.org/10.1007/s10722-010-9618-9
  2. Song Z, Kong KF, Wu H, Maricic N, Ramalingam B, Priestap H, Quirke JME, Hoiby N, Mathee K. Panax ginseng has anti-infective activity against opportunistic pathogen Pseudomonas aeruginosa by inhibiting quorum sensing, a bacterial communication process critical for establishing infection. Phytomedicine 2010;17:1040-6. https://doi.org/10.1016/j.phymed.2010.03.015
  3. Shen L, Xu J, Dong LL, Li XW, Chen SL. Cropping system and research strategies in Panax ginseng. China J Chin Mater Med 2015;40:3367-73 [in Chinese].
  4. Koide RT. Mycorrhizal symbiosis and plant reproduction. Arbuscular mycorrhizas: physiology & function. Netherlands: Springer; 2010. p. 297-320.
  5. Achatz M, Morris EK, Muller F, Hilker M, Rillig MC, Field K. Soil hyphamediated movement of allelochemicals: arbuscular mycorrhizae extend the bioactive zone of juglone. Funct Ecol 2014;28:1020-9. https://doi.org/10.1111/1365-2435.12208
  6. Felle HH, Waller F, Molitor A, Kogel KH. The mycorrhiza fungus Piriformospora indica induces fast root-surface ph signaling and primes systemic alkalinization of the leaf apoplast upon powdery mildew infection. Mol Plant Microbe In 2009;22:1179-85. https://doi.org/10.1094/MPMI-22-9-1179
  7. Geneva M, Hristozkova M, Yonova P, Boychinova M, Stancheva I. Effect of endomycorrhizal colonization with Glomus intraradices on growth and antioxidant capacity of Sideritis scardica Griseb. Gen Appl Plant Physiol 2010:47-54.
  8. Wu QS, Srivastava AK, Zou YN. AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic-Amsterdam 2013;164:77-87. https://doi.org/10.1016/j.scienta.2013.09.010
  9. Yang Y, Han X, Liang Y, Amit G, Chen J, Tang M. The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PloS One 2015;10, e0145726. https://doi.org/10.1371/journal.pone.0145726
  10. Ahmad P, Mishra RK, Mishra V, Pandey H, Pandey AC, Sharma S, Dikshit A. Mycorrhizal symbiosis. In: Ahmad P, editor. Water stress and crop plants: a sustainable approach. New Jesey: John Wiley & Sons, Ltd; 2016. p. 558-81.
  11. Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK. An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 2013;15:1870-81. https://doi.org/10.1111/1462-2920.12081
  12. Xavier LJC, Germida JJ. Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 2003;35:471-8. https://doi.org/10.1016/S0038-0717(03)00003-8
  13. Sikes BA, Klironomos J. Plant pathogen protection by AMF is determined by both root system architecture and fungal identity. 2008. ESA Annual Convention. 93rd.
  14. Fournier A, Khanizadeh S, Gauthier L, Gosselin A, Dorais M. Effect of two Glomus species inoculations on survival, photosynthetic capacity, growth, morphology and root ginsenoside content of Panax quinquefolius L. J Gins Res 2003;27:178-82. https://doi.org/10.5142/JGR.2003.27.4.178
  15. Thomas SC. Effects of vesicular-arbuscular mycorrhizae on the growth of American ginseng. J Gins Res 1995;19:73-6.
  16. Cho EJ, Lee DJ, Chi DW, Hong LK, Yong HC, Ju SC, Bo KS. Effects of AMF inoculation on growth of Panax ginseng C.A. Meyer seedlings and on soil structures in mycorrhizosphere. Sci Hortic-Amsterdam 2009;122:633-7. https://doi.org/10.1016/j.scienta.2009.06.025
  17. Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J. Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 2005;16:61-6. https://doi.org/10.1007/s00572-005-0014-9
  18. Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 1970;55:158-62. https://doi.org/10.1016/S0007-1536(70)80110-3
  19. Zhang X, Huang G, Bian X, Zhao Q. Effects of root interaction and nitrogen fertilization on the chlorophyll content, root activity, photosynthetic characteristics of intercropped soybean and microbial quantity in the rhizosphere. Plant Soil Environ 2013;59:80-8. https://doi.org/10.17221/613/2012-PSE
  20. Cohen G, Dembiec D, Marcus J. Measurement of catalase activity in tissue extracts. Anal Biochem 1970;34:30-8. https://doi.org/10.1016/0003-2697(70)90083-7
  21. Holzapfel C, Shahrokh P, Kafkewitz D. Polyphenol oxidase activity in the roots of seedlings of Bromus (Poaceae) and other grass genera. Am J Bot 2010;97:1195-9. https://doi.org/10.3732/ajb.0900337
  22. Lim Wansang, Mudge KW, Vermeylen F. Effects of population, age, and cultivation methods on ginsenoside content of wild American ginseng (Panax quinquefolium). J Agri Food Chem 2005;53:8498-505. https://doi.org/10.1021/jf051070y
  23. Tian L, Zhou X, Ma L, Xu S, Nasir F, Tian C. Root-associated bacterial diversities of Oryza rufipogon and Oryza sativa and their influencing environmental factors. Arch Microbiol 2016;199:563-71.
  24. Zhang B, Gao Q, Xu S, Tian LMC. Long-term effect of residue return and fertilization on microbial biomass and community composition of a clay loam soil. J Agr Sci Cambridg 2016;154:1051-61. https://doi.org/10.1017/S0021859615001008
  25. Kil Y-J, Eo J-K, Lee E-H, Eom A-H. Root age-dependent changes in arbuscular mycorrhizal fungal communities colonizing roots of Panax ginseng. Mycobiology 2014;42:416-21. https://doi.org/10.5941/MYCO.2014.42.4.416
  26. Sohn Jin, Lee. Distribution of arbuscular mycorrhizal fungi(AMF) at ginseng cultivated fields in Jeonnam Province. Korean J Soil Sci Fertil 2008;41.
  27. Della Monica IF, Saparrat MCN, Godeas AM, Scervino JM. The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes. Fungal Ecol 2015;17:10-7. https://doi.org/10.1016/j.funeco.2015.04.004
  28. Liu Z, Li Y,Ma L,Wei H, Zhang J,He X, Tian C. Coordinated regulation of arbuscular mycorrhizal fungi and soybean MAPK pathway genes improved mycorrhizal soybean drought tolerance. Mol Plant Microbe In 2015;28:408. https://doi.org/10.1094/MPMI-09-14-0251-R
  29. Liu Z, Ma L, He X, Tian C. Water strategy of mycorrhizal rice at low temperature through the regulation of PIP aquaporins with the involvement of trehalose. Appl Soil Ecol 2014;84:185-91. https://doi.org/10.1016/j.apsoil.2014.07.010
  30. Wu J, Zhong JJ. Production of ginseng and its bioactive components in plant cell culture: current technological and applied aspects. J Biotechnol 1999;68:89-99. https://doi.org/10.1016/S0168-1656(98)00195-3
  31. Ghazanfar B, Zhihui C, Wu C, Liu H, Li H, Rehman RNU, Ahmad I, Khan AR. Glomus etunicatum root inoculation and foliar application of acetyl salicylic acid induced nacl tolerance by regulation of Nac1 & Lenhx1 gene expression and improved photosynthetic performance in tomato seedlings. Pak J Bot 2016;48:1209-17.
  32. Minton MM, Barber NA, Gordon LL. Effects of arbuscular mycorrhizal fungi on herbivory defense in two Solanum (Solanaceae) species. Plant Ecol Evol 2016.
  33. You ZM, Zhao L, Xia J, Wei Q, Liu YM, Liu XY, Chen DL, Li J. Down-regulation of phosphoglucose isomerase/autocrine motility factor enhances gensenoside Rh2 pharmacological action on leukemia KG1 cells. Asian Pac J Cancer P 2014;15:1099-104. https://doi.org/10.7314/APJCP.2014.15.3.1099
  34. MFd Silva, Pescador R, Rebelo RA, Sturmer SL. The effect of arbuscular mycorrhizal fungal isolates on the development and oleoresin production of micropropagated Zingiber officinale. Braz J Plant Physiol 2008;20:119-30. https://doi.org/10.1590/S1677-04202008000200004
  35. Punja ZK. Fungal pathogens of american ginseng (Panax quinquefolium) in British columbia. Can J Plant Pathol 1997;19:301-6. https://doi.org/10.1080/07060669709500528
  36. Sharma A, Johri BN, Sharma AK, Glick BR. Plant growth-promoting bacterium Pseudomonas sp. strain GRP3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol Biochem 2003;35:887-94. https://doi.org/10.1016/S0038-0717(03)00119-6
  37. Mechri B, Manga AGB, Tekaya M, Attia F, Cheheb H, Meriem FB, Braham M, Boujnah D, Hammami M. Changes in microbial communities and carbohydrate profiles induced by the mycorrhizal fungus (Glomus intraradices ) in rhizosphere of olive trees (Olea europaea L.). Appl Soil Ecol 2014;75:124-33. https://doi.org/10.1016/j.apsoil.2013.11.001
  38. Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M. The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plantarum 2001;111:206-11. https://doi.org/10.1034/j.1399-3054.2001.1110211.x
  39. Pueppke SG, Broughton WJ. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant Microbe In 1999;12:293-318. https://doi.org/10.1094/MPMI.1999.12.4.293
  40. Gao J, Wang Y, Wang CW, Lu BH. First report of bacterial root rot of ginseng caused by Pseudomonas aeruginosa in China [Disease Notes]. Plant Dis 2014;98:1577.
  41. Garibaldi A, Bertetti D, Moretti C, Buonaurio R, Gullino ML. First report of bacterial blight caused by an unknown Erwinia sp. on Verbenahybrida in Italy [Disease Notes]. J Plant Pathol 2011;93:243.
  42. Sayeed AM, Zakia S. Biocontrol of a root-rot disease complex of chickpea by Glomus intraradices, Rhizobium sp. and Pseudomonas straita. Crop Prot 2008;27:410-7. https://doi.org/10.1016/j.cropro.2007.07.009
  43. Kim JH, Lee MW, Kim GP. Studies on the root rot of ginseng - (IV) distribution of fungi and Fusarium sp. population in ginseng cultivation soil. J Endocrinol 1974;2:279-80.
  44. Lee JH, Yu YH, Kim YH, Ohh SH, Park WM. Morphological characteristics and pathogenicity of Alternaria isolates causing leaf and stem blights and black root rot of Korea ginseng. Korean J Plant Pathol 1990:13-20.
  45. Kjoller R, Rosendahl S. The presence of the arbuscular mycorrhizal fungus Glomus intraradices influences enzymatic activities of the root pathogen Aphanomyces euteiches in pea roots. Mycorrhiza 1997;6:487-91. https://doi.org/10.1007/s005720050152

Cited by

  1. Effect of the biocontrol bacterium Bacillus amyloliquefaciens on the rhizosphere in ginseng plantings vol.21, pp.3, 2019, https://doi.org/10.1007/s10123-018-0015-0
  2. Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae vol.12, 2019, https://doi.org/10.1186/s12284-019-0287-9
  3. Research Advances of Beneficial Microbiota Associated with Crop Plants vol.21, pp.5, 2019, https://doi.org/10.3390/ijms21051792
  4. Fungicides alter the distribution and diversity of bacterial and fungal communities in ginseng fields vol.12, pp.1, 2019, https://doi.org/10.1080/21655979.2021.1982277
  5. Microbial Biostimulants as Response to Modern Agriculture Needs: Composition, Role and Application of These Innovative Products vol.10, pp.8, 2019, https://doi.org/10.3390/plants10081533
  6. Effects of arbuscular mycorrhizal fungi on photosynthesis and biosynthesis of ginsenoside in Panax quinquefolius L. vol.33, pp.3, 2021, https://doi.org/10.1007/s40626-021-00208-y
  7. The Effect of Rhizophagus irregularis, Bacillus subtilis and Water Regime on the Plant-Microbial Soil System: The Case of Lactuca sativa vol.11, pp.11, 2019, https://doi.org/10.3390/agronomy11112183