DOI QR코드

DOI QR Code

Changes in Endophyte Communities across the Different Plant Compartments in Response to the Rice Blast Infection

  • Received : 2023.12.21
  • Accepted : 2024.04.17
  • Published : 2024.06.01

Abstract

The rice blast disease, caused by the fungal pathogen, Magnaporthe oryzae (syn. Pyricularia oryzae), poses a significant threat to the global rice production. Understanding how this disease impacts the plant's microbial communities is crucial for gaining insights into host-pathogen interactions. In this study, we investigated the changes in communities of bacterial and fungal endophytes inhabiting different compartments in healthy and diseased plants. We found that both alpha and beta diversities of endophytic communities do not change significantly by the pathogen infection. Rather, the type of plant compartment appeared to be the main driver of endophytic community structures. Although the overall structure seemed to be consistent between healthy and diseased plants, our analysis of differentially abundant taxa revealed the specific bacterial and fungal operational taxonomic units that exhibited enrichment in the root and leaf compartments of infected plants. These findings suggest that endophyte communities are robust to the changes at the early stage of pathogen infection, and that some of endophytes enriched in infected plants might have roles in the defense against the pathogen.

Keywords

Acknowledgement

This work was supported by a grant from the National Research Foundation of Korea (NRF-2018R1A5A1023599), and by a grant from Rural Development Administration (PJ013178).

References

  1. Bakker, P. A. H. M., Pieterse, C. M., De Jonge, R. and Berendsen, R. L. 2018. The soil-borne legacy. Cell 172:1178-1180. https://doi.org/10.1016/j.cell.2018.02.024
  2. Ballini, E., Nguyen, T. T. and Morel, J.-B. 2013. Diversity and genetics of nitrogen-induced susceptibility to the blast fungus in rice and wheat. Rice 6:32.
  3. Banerjee, M. and Yesmin, L. 2002. Sulfur-oxidizing plant growth promoting rhizobacteria for enhanced canola performance. US Patent 07491535. U.S. Patent and Trademark Office, Washington, DC, USA.
  4. Barrett, C. B. 2021. Overcoming global food security challenges through science and solidarity. Am. J. Agric. Econ. 103:422-447. https://doi.org/10.1111/ajae.12160
  5. Berg, G., Grube, M., Schloter, M. and Smalla, K. 2014. Unraveling the plant microbiome: looking back and future perspectives. Front. Microbiol. 5:148.
  6. Berg, G., Marten, P. and Ballin, G. 1996. Stenotrophomonas maltophilia in the rhizosphere of oilseed rape: occurrence, characterization and interaction with phytopathogenic fungi. Microbiol. Res. 151:19-27. https://doi.org/10.1016/S0944-5013(96)80051-6
  7. Berruyer, R., Adreit, H., Milazzo, J., Gaillard, S., Berger, A., Dioh, W., Lebrun, M.-H. and Tharreau, D. 2003. Identification and fine mapping of Pi33, the rice resistance gene corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor. Appl. Genet. 107:1139-1147. https://doi.org/10.1007/s00122-003-1349-2
  8. Bertani, I., Abbruscato, P., Piffanelli, P., Subramoni, S. and Venturi, V. 2016. Rice bacterial endophytes: isolation of a collection, identification of beneficial strains and microbiome analysis. Environ. Microbiol. Rep. 8:388-398. https://doi.org/10.1111/1758-2229.12403
  9. Bulgarelli, D., Schlaeppi, K., Spaepen, S., Van Themaat, E. V. L. and Schulze-Lefert, P. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807-838. https://doi.org/10.1146/annurev-arplant-050312-120106
  10. Busby, P. E., Soman, C., Wagner, M. R., Friesen, M. L., Kremer, J., Bennett, A., Morsy, M., Eisen, J. A., Leach, J. E. and Dangl, J. L. 2017. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol. 15:e2001793.
  11. Chen, M., Chen, J., Liu, J., Wu, M., Yan, Q., Li, P., Huang, L. and Xiao, X. 2021. Diversity analysis of rhizosphere soil fungi and endophytic fungi in Ampelocalamus luodianensis. Acta Ecol. Sin. 41:4120-4130.
  12. Compant, S., Nowak, J., Coenye, T., Clement, C. and Ait Barka, E. 2008. Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol. Rev. 32:607-626. https://doi.org/10.1111/j.1574-6976.2008.00113.x
  13. Cummings, N. J., Ambrose, A., Braithwaite, M., Bissett, J., Roslan, H. A., Abdullah, J., Stewart, A., Agbayani, F. V., Steyaert, J. and Hill, R. A. 2016. Diversity of root-endophytic Trichoderma from Malaysian Borneo. Mycol. Prog. 15:50.
  14. Dastogeer, K. M. G., Tumpa, F. H., Sultana, A., Akter, M. A. and Chakraborty, A. 2020. Plant microbiome: an account of the factors that shape community composition and diversity. Curr. Plant Biol. 23:100161.
  15. Dedysh, S. N., Haupt, E. S. and Dunfield, P. F. 2016. Emended description of the family Beijerinckiaceae and transfer of the genera Chelatococcus and Camelimonas to the family Chelatococcaceae fam. nov. Int. J. Syst. Evol. Microbiol. 66:3177-3182. https://doi.org/10.1099/ijsem.0.001167
  16. Devanna, B. N., Jain, P., Solanke, A. U., Das, A., Thakur, S., Singh, P. K., Kumari, M., Dubey, H., Jaswal, R., Pawar, D., Kapoor, R., Singh, J., Arora, K., Saklani, B. K., AnilKumar, C., Maganti, S. M., Sonah, H., Deshmukh, R., Rathour, R. and Sharma, T. R. 2022. Understanding the dynamics of blast resistance in rice: Magnaporthe oryzae interactions. J. Fungi 8:584.
  17. Duan, G., Li, C., Liu, Y., Ma, X., Luo, Q. and Yang, J. 2021. Magnaporthe oryzae systemic defense trigger 1 (MoSDT1)-mediated metabolites regulate defense response in rice. BMC Plant Biol. 21:40.
  18. Elbeltagy, A., Nishioka, K., Suzuki, H., Sato, T., Sato, Y.-I., Morisaki, H., Mitsui, K. and Minamisawa, K. 2000. Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci. Plant Nutr. 46:617-629. https://doi.org/10.1080/00380768.2000.10409127
  19. Friesen, M. L., Porter, S. S., Stark, S. C., von Wettberg, E. J., Sachs, J. L. and Martinez-Romero, E. 2011. Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42:23-46. https://doi.org/10.1146/annurev-ecolsys-102710-145039
  20. Hardoim, P. R., Hardoim, C. C. P., van Overbeek, L. S. and van Elsas, J. D. 2012. Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7:e30438.
  21. Jakuschkin, B., Fievet, V., Schwaller, L., Fort, T., Robin, C. and Vacher, C. 2016. Deciphering the pathobiome: intra- and interkingdom interactions involving the pathogen Erysiphe alphitoides. Microb. Ecol. 72:870-880. https://doi.org/10.1007/s00248-016-0777-x
  22. Juhnke, M. E. and des Jardin, E. 1989. Selective medium for isolation of Xanthomonas maltophilia from soil and rhizosphere environments. Appl. Environ. Microbiol. 55:747-750. https://doi.org/10.1128/aem.55.3.747-750.1989
  23. Kai, M., Effmert, U., Berg, G. and Piechulla, B. 2007. Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch. Microbiol. 187:351-360. https://doi.org/10.1007/s00203-006-0199-0
  24. Khan, A. L., Waqas, M., Kang, S.-M., Al-Harrasi, A., Hussain, J., Al-Rawahi, A., Al-Khiziri, S., Ullah, I., Ali, L., Jung, H.-Y. and Lee, I.-J. 2014. Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J. Microbiol. 52:689-695. https://doi.org/10.1007/s12275-014-4002-7
  25. Khush, G. 2003. Productivity improvements in rice. Nutr. Rev. 61:S114-S116. https://doi.org/10.1301/nr.2003.jun.S114-S116
  26. Kirtphaiboon, S., Humphries, U., Khan, A. and Yusuf, A. 2021. Model of rice blast disease under tropical climate conditions. Chaos Solitons Fract. 143:110530.
  27. Lamprecht, S. C., Tewoldemedhin, Y. T., Botha, W. J. and Calitz, F. J. 2011. Fusarium graminearum species complex associated with maize crowns and roots in the KwaZulu-Natal province of South Africa. Plant Dis. 95:1153-1158. https://doi.org/10.1094/PDIS-02-11-0083
  28. Liba, C. M., Ferrara, F. I. S., Manfio, G. P., Fantinatti-Garboggini, F., Albuquerque, R. C., Pavan, C., Ramos, P. L., Moreira-Filho, C. A. and Barbosa, H. R. 2006. Nitrogen-fixing chemo-organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J. Appl. Microbiol. 101:1076-1086. https://doi.org/10.1111/j.1365-2672.2006.03010.x
  29. Liu, H., Brettell, L. E., Qiu, Z. and Singh, B. K. 2020. Microbiome-mediated stress resistance in plants. Trends Plant Sci. 25:733-743. https://doi.org/10.1016/j.tplants.2020.03.014
  30. Liu, H., Macdonald, C. A., Cook, J., Anderson, I. C. and Singh, B. K. 2019. An ecological loop: host microbiomes across multitrophic interactions. Trends Ecol. Evol. 34:1118-1130. https://doi.org/10.1016/j.tree.2019.07.011
  31. Love, M. I., Huber, W. and Anders, S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550.
  32. Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D. and Dangl, J. L. 2013. Practical innovations for high-throughput amplicon sequencing. Nat. Methods 10:999-1002. https://doi.org/10.1038/nmeth.2634
  33. Ma, K.-W., Niu, Y., Jia, Y., Ordon, J., Copeland, C., Emonet, A., Geldner, N., Guan, R., Stolze, S. C., Nakagami, H., Garrido-Oter, R. and Schulze-Lefert, P. 2021. Coordination of microbe-host homeostasis by crosstalk with plant innate immunity. Nat. Plants 7:814-825. https://doi.org/10.1038/s41477-021-00920-2
  34. Mannaa, M. and Seo, Y.-S. 2021. Plants under the attack of allies: moving towards the plant pathobiome paradigm. Plants 10:125.
  35. Mano, H. and Morisaki, H. 2008. Endophytic bacteria in the rice plant. Microbes Environ. 23:109-117. https://doi.org/10.1264/jsme2.23.109
  36. Mc Carthy, U., Uysal, I., Badia-Melis, R., Mercier, S., O'Donnell, C. and Ktenioudaki, A. 2018. Global food security: issues, challenges and technological solutions. Trends Food Sci. Technol. 77:11-20. https://doi.org/10.1016/j.tifs.2018.05.002
  37. Mercado-Blanco, J. and Lugtenberg, B. J. J. 2014. Biotechnological applications of bacterial endophytes. Curr. Biotechnol. 3:60-75. https://doi.org/10.2174/22115501113026660038
  38. Mousa, W. K., Shearer, C. R., Limay-Rios, V., Zhou, T. and Raizada, M. N. 2015. Bacterial endophytes from wild maize suppress Fusarium graminearum in modern maize and inhibit mycotoxin accumulation. Front. Plant Sci. 6:805.
  39. Musonerimana, S., Bez, C., Licastro, D., Habarugira, G., Bigirimana, J. and Venturi, V. 2020. Pathobiomes revealed that Pseudomonas fuscovaginae and Sarocladium oryzae are independently associated with rice sheath rot. Microb. Ecol. 80:627-642. https://doi.org/10.1007/s00248-020-01529-2
  40. Nguyen, Q. T., Ueda, K., Kihara, J. and Ueno, M. 2016. Culture filtrates of Trichoderma isolate H921 inhibit Magnaporthe oryzae spore germination and blast lesion formation in rice. Adv. Microbiol. 6:521-527. https://doi.org/10.4236/aim.2016.67052
  41. Oerke, E.-C. 2006. Crop losses to pests. J. Agric. Sci. 144:31-43. https://doi.org/10.1017/S0021859605005708
  42. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. 2018. vegan: Community Ecology Package. R package version 2.5-3. URL https://CRAN.R-project.org/web/packages/vegan/index.html [21 December 2023].
  43. Park, M., Kim, C., Yang, J., Lee, H., Shin, W., Kim, S. and Sa, T. 2005. Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol. Res. 160:127-133. https://doi.org/10.1016/j.micres.2004.10.003
  44. Philippot, L., Raaijmakers, J. M., Lemanceau, P. and van der Putten, W. H. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11:789-799. https://doi.org/10.1038/nrmicro3109
  45. Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. and Van Wees, S. C. M. 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521. https://doi.org/10.1146/annurev-cellbio-092910-154055
  46. Richards, D. E., King, K. E., Ait-Ali, T. and Harberd, N. P. 2001. How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signalling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 526:67-88.
  47. Rosenblueth, M. and Martinez-Romero, E. 2006. Bacterial endophytes and their interactions with hosts. Mol. Plant-Microbe Interact. 19:827-837. https://doi.org/10.1094/MPMI-19-0827
  48. Santos, L. F. and Olivares, F. L. 2021. Plant microbiome structure and benefits for sustainable agriculture. Curr. Plant Biol. 26:100198.
  49. Scholthof, H. B. 2001. Molecular plant-microbe interactions that cut the mustard. Plant Physiol. 127:1476-1483. https://doi.org/10.1104/pp.010789
  50. Schulz, B., Guske, S., Dammann, U. and Boyle, C. 1998. Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213-227.
  51. Shanmugam, G., Lee, S. H. and Jeon, J. 2021. EzMAP: Easy Microbiome Analysis Platform. BMC Bioinformatics 22:179.
  52. Skamnioti, P. and Gurr, S. J. 2009. Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol. 27:141-150. https://doi.org/10.1016/j.tibtech.2008.12.002
  53. Song, C., Zhu, F., Carrion, V. J. and Cordovez, V. 2020. Beyond plant microbiome composition: exploiting microbial functions and plant traits via integrated approaches. Front. Bioeng. Biotechnol. 8:896.
  54. Stotzky, G. and Schenck, S. 1976. Volatile organic compounds and microorganisms. Crit. Rev. Microbiol. 4:333-382. https://doi.org/10.3109/10408417609102303
  55. Suckstorff, I. and Berg, G. 2003. Evidence for dose-dependent effects on plant growth by Stenotrophomonas strains from different origins. J. Appl. Microbiol. 95:656-663. https://doi.org/10.1046/j.1365-2672.2003.02021.x
  56. Teixeira, P. J. P. L., Colaianni, N. R., Law, T. F., Conway, J. M., Gilbert, S., Li, H., Salas-Gonzalez, I., Panda, D., Del Risco, N. M., Finkel, O. M., Castrillo, G., Mieczkowski, P., Jones, C. D. and Dangl, J. L. 2021. Specific modulation of the root immune system by a community of commensal bacteria. Proc. Natl. Acad. Sci. 118:e2100678118.
  57. Tian, X., Cao, L., Tan, H., Han, W., Chen, M., Liu, Y. and Zhou, S. 2007. Diversity of cultivated and uncultivated actinobacterial endophytes in the stems and roots of rice. Microb. Ecol. 53:700-707. https://doi.org/10.1007/s00248-006-9163-4
  58. Trivedi, P., Batista, B. D., Bazany, K. E. and Singh, B. K. 2022. Plant-microbiome interactions under a changing world: responses, consequences and perspectives. New Phytol. 234:1951-1959. https://doi.org/10.1111/nph.18016
  59. Tyskiewicz, R., Nowak, A., Ozimek, E. and Jaroszuk-Scisel, J. 2022. Trichoderma: the current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. Int. J. Mol. Sci. 23:2329.
  60. Valent, B. 2021. The impact of blast disease: past, present, and future in Magnaporthe oryzae. Methods Mol. Biol. 2356:1-18. https://doi.org/10.1007/978-1-0716-1613-0_1
  61. Vannier, N., Agler, M. and Hacquard, S. 2019. Microbiota-mediated disease resistance in plants. PLoS Pathog. 15:e1007740.
  62. Vurukonda, S. S. K. P., Giovanardi, D. and Stefani, E. 2018. Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int. J. Mol. Sci. 19:952.
  63. Walitang, D. I., Kim, K., Madhaiyan, M., Kim, Y. K., Kang, Y. and Sa, T. 2017. Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of rice. BMC Microbiol. 17:209.
  64. Wang, W., Zhai, Y., Cao, L., Tan, H. and Zhang, R. 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
  65. Wei, Y., Li, L., Hu, W., Ju, H., Zhang, M., Qin, Q., Zhang, S. and Li, G. 2020. Suppression of rice blast by bacterial strains isolated from cultivated soda saline-sodic soils. Int. J. Environ. Res. Public Health 17:5248.
  66. Wheatley, R. E. 2002. The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357-364. https://doi.org/10.1023/A:1020592802234
  67. Zhang, J., Cook, J., Nearing, J. T., Zhang, J., Raudonis, R., Glick, B. R., Langille, M. G. I. and Cheng, Z. 2021. Harnessing the plant microbiome to promote the growth of agricultural crops. Microbiol. Res. 245:126690.
  68. Zheng, W., Tsompana, M., Ruscitto, A., Sharma, A., Genco, R., Sun, Y. and Buck, M. J. 2015. An accurate and efficient experimental approach for characterization of the complex oral microbiota. Microbiome 3:48.