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MicroRNAs Involved in Nutritional Regulation During Plant–Microbe Symbiotic and Pathogenic Interactions with Rice as a Model

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Abstract

Plants are constantly challenged with numerous adverse environmental conditions, including biotic and abiotic stresses. Coordinated regulation of plant responses requires crosstalk between regulatory pathways initiated by different external cues. Stress induced by excessiveness or deficiency of nutrients has been shown to positively or negatively interact with pathogen-induced immune responses. Also, colonization by arbuscular mycorrhizal (AM) fungi can improve plant nutrition, mainly phosphorus and resistance to pathogen infection. The proposed review addresses these issues about a new question that integrates adaptation to nutrient stress and disease resistance. The main goal of the current review is to provide insights into the interconnected regulation between nutrient signaling and immune signaling pathways in rice, focusing on phosphate, potassium and iron signaling. The underpinnings of plant/pathogen/AM fungus interaction concerning rice/M. oryzae/R. irregularis is highlighted. The role of microRNAs (miRNAs) involved in Pi (miR399, miR827) and Fe (miR7695) homeostasis in pathogenic/symbiotic interactions in rice is discussed. The intracellular dynamics of membrane proteins that function in nutrient transport transgenic rice lines expressing fluorescent protein fusion genes are outlined. Integrating functional genomic, nutritional and metal content, molecular and cell biology approaches to understand how disease resistance is regulated by nutrient status leading to novel concepts in fundamental processes underlying plant disease resistance will help to devise novel strategies for crop protection with less input of pesticides and fertilizers.

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References

  1. Markandan, K., & Chai, W. S. (2022). Perspectives on nanomaterials and nanotechnology for sustainable bioenergy generation. Materials, 15, 7769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Singh, B. K., Delgado-Baquerizo, M., Egidi, E., et al. (2023). Climate change impacts on plant pathogens, food security and paths forward. Nature Reviews Microbiology. https://doi.org/10.1038/s41579-023-00900-7

    Article  PubMed  PubMed Central  Google Scholar 

  3. Veresoglou, S. D., Barto, E. K., Menexes, G., & Rillig, M. C. (2013). Fertilization affects severity of disease caused by fungal plant pathogens. Plant Pathology, 62, 961–969.

    Article  Google Scholar 

  4. Bonfante, P., & Genre, A. (2010). Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nature Communications, 1, 1–11.

    Article  Google Scholar 

  5. Parniske, M. (2008). Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nature Reviews Microbiology, 6, 763–775.

    Article  CAS  PubMed  Google Scholar 

  6. Yadav, R., Ror, P., Beniwal, R., Kumar, S., & Ramakrishna, W. (2022). Bacillus sp. and arbuscular mycorrhizal fungi consortia enhance wheat nutrient and yield in the second-year field trial: Superior performance in comparison with chemical fertilizers. Journal of Applied Microbiology, 132, 2203–2219.

    Article  CAS  PubMed  Google Scholar 

  7. Sawers, R. J., Ramírez-Flores, M. R., Olalde-Portugal, V., & Paszkowski, U. (2018). The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: Insights from genetics and genomics. New Phytologist, 220, 1135–1140.

    Article  PubMed  Google Scholar 

  8. Lanfranco, L., Fiorilli, V., & Gutjahr, C. (2018). Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytologist, 220, 1031–1046.

    Article  PubMed  Google Scholar 

  9. Wilson, R. A., & Talbot, N. J. (2009). Under pressure: Investigating the biology of plant infection by Magnaporthe oryzae. Nature Reviews Microbiology, 7, 185–195.

    Article  CAS  PubMed  Google Scholar 

  10. Ballini, E., Nguyen, T. T., & Morel, J. B. (2013). Diversity and genetics of nitrogen-induced susceptibility to the blast fungus in rice and wheat. Rice, 6, 1–13.

    Article  Google Scholar 

  11. Miller, S. S., Dornbusch, M. R., Farmer, A. D., Huertas, R., Gutierrez-Gonzalez, J. J., Young, N. D., Samac, D. A., & Curtin, S. J. (2022). Alfalfa (Medicago sativa L.) pho2 mutant plants hyperaccumulate phosphate. G3, 12, jkac096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sánchez-Sanuy, F., Peris-Peris, C., Tomiyama, S., Okada, K., Hsing, Y. I., San Segundo, B., & Campo, S. (2019). Osa-miR7695 enhances transcriptional priming in defense responses against the rice blast fungus. BMC Plant Biology, 19, 1–16.

    Article  Google Scholar 

  13. Shi, X., Long, Y., He, F., Zhang, C., Wang, R., Zhang, T., Wu, W., Hao, Z., Wang, Y. I., Wang, G. L., & Ning, Y. (2018). The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel. PLoS Pathogens, 14, e1006878.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Paul, S., Datta, S. K., & Datta, K. (2015). miRNA regulation of nutrient homeostasis in plants. Frontiers in Plant Science, 6, 232.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., & Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320, 1185–1190.

    Article  CAS  PubMed  Google Scholar 

  16. Chen, X. (2009). Small RNAs and their roles in plant development. Annual Review of Cell and Developmental Biology, 25, 21.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Song, X., Li, Y., Cao, X., & Qi, Y. (2019). MicroRNAs and their regulatory roles in plant–environment interactions. Annual Review of Plant Biology, 70, 489–525.

    Article  CAS  PubMed  Google Scholar 

  18. Chien, P. S., Chiang, C. B., Wang, Z., & Chiou, T. J. (2017). MicroRNA-mediated signaling and regulation of nutrient transport and utilization. Current Opinion in Plant Biology, 39, 73–79.

    Article  CAS  PubMed  Google Scholar 

  19. Puga, M. I., Rojas-Triana, M., de Lorenzo, L., Leyva, A., Rubio, V., & Paz-Ares, J. (2017). Novel signals in the regulation of Pi starvation responses in plants: Facts and promises. Current Opinion in Plant Biology, 39, 40–49.

    Article  CAS  PubMed  Google Scholar 

  20. Batstone, R. T. (2022). Genomes within genomes: Nested symbiosis and its implications for plant evolution. New Phytologist, 234, 28–34.

    Article  CAS  PubMed  Google Scholar 

  21. Sun, Y., Wang, M., Mur, L. A. J., Shen, Q., & Guo, S. (2021). The cross-kingdom roles of mineral nutrient transporters in plant-microbe relations. Physiologia Plantarum, 171, 771–784.

    Article  CAS  PubMed  Google Scholar 

  22. Liu, Q., Zhang, C., Fang, H., Yi, L., & Li, M. (2023). Indispensable biomolecules for plant defense against pathogens: NBS-LRR and “nitrogen pool” alkaloids. Plant Science, 334, 111752.

    Article  CAS  PubMed  Google Scholar 

  23. Morinière, L., Mirabel, L., Gueguen, E., & Bertolla, F. (2022). A comprehensive overview of the genes and functions required for lettuce infection by the hemibiotrophic phytopathogen Xanthomonas hortorum pv. vitians. Msystems, 7, e01290-e1321.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Li, Y., Zhao, S. L., Li, J. L., Hu, X. H., Wang, H., Cao, X. L., Xu, Y. J., Zhao, Z. X., Xiao, Z. Y., Yang, N., & Fan, J. (2017). Osa-miR169 negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Frontiers in Plant Science, 8, 2.

    PubMed  PubMed Central  Google Scholar 

  25. Jiang, J., Zhu, H., Li, N., Batley, J., & Wang, Y. (2022). The miR393-target module regulates plant development and responses to biotic and abiotic Stresses. International Journal of Molecular Sciences, 23, 9477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gan, Q., Song, F., Zhang, C., Han, Z., Teng, B., Lin, C., Gu, D., Wang, J., Pei, H., Wu, J., & Fang, J. (2023). Ca2+ deficiency triggers panicle degeneration in rice mediated by Ca2+/H+ exchanger OsCAX1a. Plant, Cell and Environment, 46, 1610–1628.

    Article  CAS  PubMed  Google Scholar 

  27. Yang, Z., Hui, S., Lv, Y., Zhang, M., Chen, D., Tian, J., Zhang, H., Liu, H., Cao, J., Xie, W., & Wu, C. (2022). miR395-regulated sulfate metabolism exploits pathogen sensitivity to sulfate to boost immunity in rice. Molecular Plant, 15, 671–688.

    Article  CAS  PubMed  Google Scholar 

  28. Julian Maywald, N., Francioli, D., Mang, M., & Ludewig, U. (2023). Role of mineral nitrogen nutrition in fungal plant diseases of cereal crops. Critical Reviews in Plant Sciences, 42, 93–123.

    Article  CAS  Google Scholar 

  29. Campos-Soriano, L., Bundó, M., Bach-Pages, M., Chiang, S. F., Chiou, T. J., & San Segundo, B. (2020). Phosphate excess increases susceptibility to pathogen infection in rice. Molecular Plant Pathology, 21, 555–570.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Paries, M., & Gutjahr, C. (2023). The good, the bad, and the phosphate: Regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status. New Phytolog., 239, 29–46.

    Article  CAS  Google Scholar 

  31. Nguyen, N. K., Wang, J., Liu, D., Hwang, B. K., & Jwa, N. S. (2022). Rice iron storage protein ferritin 2 (OsFER2) positively regulates ferroptotic cell death and defense responses against Magnaporthe oryzae. Frontiers in Plant Science, 13, 1019669.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Filipe, O., De Vleesschauwer, D., Haeck, A., Demeestere, K., & Höfte, M. (2018). The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice. Science and Reports, 8, 3864.

    Article  Google Scholar 

  33. Kim, C.-Y., Vo, K. T. X., An, G., & Jeon, J.-S. (2015). A rice sucrose non-fermenting-1 related protein kinase 1, OSK35, plays an important role in fungal and bacterial disease resistance. Journal of the Korean Society for Applied Biological Chemistry, 58, 669–675.

    Article  CAS  Google Scholar 

  34. Eichmann, R., & Schäfer, P. (2015). Growth versus immunity—A redirection of the cell cycle? Current Opinion in Plant Biology, 26, 106–112.

    Article  CAS  PubMed  Google Scholar 

  35. Tamaoki, D., Seo, S., Yamada, S., Kano, A., Miyamoto, A., Shishido, H., Miyoshi, S., Taniguchi, S., Akimitsu, K., & Gomi, K. (2013). Jasmonic acid and salicylic acid activate a common defense system in rice. Plant Signaling & Behavior, 8, e24260.

    Article  Google Scholar 

  36. Liu, P., Guo, J., Zhang, R., Zhao, J., Liu, C., Qi, T., Duan, Y., Kang, Z., & Guo, J. (2019). TaCIPK10 interacts with and phosphorylates TaNH2 to activate wheat defense responses to stripe rust. Plant Biotechnology Journal, 17, 956–968.

    Article  CAS  PubMed  Google Scholar 

  37. Sardar, A., Nandi, A. K., & Chattopadhyay, D. (2017). CBL-interacting protein kinase 6 negatively regulates immune response to Pseudomonas syringae in Arabidopsis. Journal of Experimental Botany, 68, 3573–3584.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kumar, S., Verma, S., & Trivedi, P. K. (2017). Involvement of small RNAs in phosphorus and sulfur sensing, signaling and stress: Current Update. Frontiers in Plant Science, 8, 285.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Val-Torregrosa, B., Bundó, M., & San Segundo, B. (2021). Crosstalk between nutrient signalling pathways and immune responses in rice. Agriculture, 11, 747.

    Article  CAS  Google Scholar 

  40. Lin, S. I., Chiang, S. F., Lin, W. Y., Chen, J. W., Tseng, C. Y., Wu, P. C., & Chiou, T. J. (2008). Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology, 147, 732–746.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Li, Y., Li, T. T., He, X. R., Zhu, Y., Feng, Q., Yang, X. M., Zhou, X. H., Li, G. B., Ji, Y. P., Zhao, J. H., & Zhao, Z. X. (2022). Blocking Osa-miR1871 enhances rice resistance against Magnaporthe oryzae and yield. Plant Biotechnology Journal, 20, 646–659.

    Article  CAS  PubMed  Google Scholar 

  42. Li, Y., Tong, Y., He, X., Zhu, Y., Li, T., Lin, X., Mao, W., Gishkori, Z. G. N., Zhao, Z., Zhang, J., & Huang, Y. (2022). The rice miR171b–SCL6-IIs module controls blast resistance, grain yield, and flowering. Crop J., 10, 117–127.

    Article  Google Scholar 

  43. Iwamoto, M. (2022). In-frame editing of transcription factor gene RDD1 to suppress miR166 recognition influences nutrient uptake, photosynthesis, and grain quality in rice. Science and Reports, 12, 1–11.

    Google Scholar 

  44. Wang, H., Li, Y., Chern, M., Zhu, Y., Zhang, L. L., Lu, J. H., Li, X. P., Dang, W. Q., Ma, X. C., Yang, Z. R., & Yao, S. Z. (2021). Suppression of rice miR168 improves yield, flowering time and immunity. Nature Plants, 7, 129–136.

    Article  CAS  PubMed  Google Scholar 

  45. Baldrich, P., Campo, S., Wu, M. T., Liu, T. T., Hsing, Y. I. C., & Segundo, B. S. (2015). MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biology, 12, 847–863.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Liu, G., Greenshields, D. L., Sammynaiken, R., Hirji, R. N., Selvaraj, G., & Wei, Y. (2007). Targeted alterations in iron homeostasis underlie plant defense responses. Journal of Cell Science, 120, 596–605.

    Article  CAS  PubMed  Google Scholar 

  47. Zhou, J., Wang, X., He, Y., Sang, T., Wang, P., Dai, S., Zhang, S., & Meng, X. (2020). Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. The Plant Cell, 32, 2621–2638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhou, S. X., Zhu, Y., Wang, L. F., Zheng, Y. P., Chen, J. F., Li, T. T., Yang, X. M., Wang, H., Li, X. P., Ma, X. C., & Zhao, J. Q. (2020). Osa-miR1873 fine-tunes rice immunity against Magnaporthe oryzae and yield traits. Journal of Integrative Plant Biology, 62, 1213–1226.

    Article  CAS  PubMed  Google Scholar 

  49. Li, X. P., Ma, X. C., Wang, H., Zhu, Y., Liu, X. X., Li, T. T., Zheng, Y. P., Zhao, J. Q., Zhang, J. W., Huang, Y. Y., & Pu, M. (2020). Osa-miR162a fine-tunes rice resistance to Magnaporthe oryzae and yield. Rice, 13, 1–13.

    Article  Google Scholar 

  50. Li, Y., Liu, X., Yin, Z., You, Y., Zou, Y., Liu, M., He, Y., Zhang, H., Zheng, X., Zhang, Z., & Wang, P. (2020). MicroRNA-like milR236, regulated by transcription factor MoMsn2, targets histone acetyltransferase MoHat1 to play a role in appressorium formation and virulence of the rice blast fungus Magnaporthe oryzae. Fungal Genetics and Biology, 137, 103349.

    Article  CAS  PubMed  Google Scholar 

  51. Zhao, Z. X., Feng, Q., Cao, X. L., Zhu, Y., Wang, H., Chandran, V., Fan, J., Zhao, J. Q., Pu, M., Li, Y., & Wang, W. M. (2020). Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. Journal of Integrative Plant Biology, 62, 702–715.

    Article  CAS  PubMed  Google Scholar 

  52. Campo, S., Peris-Peris, C., Siré, C., Moreno, A. B., Donaire, L., Zytnicki, M., Notredame, C., Llave, C., & San Segundo, B. (2013). Identification of a novel micro-RNA (mi RNA) from rice that targets an alternatively spliced transcript of the N ramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytologist, 199, 212–227.

    Article  CAS  PubMed  Google Scholar 

  53. Campo, S., Sánchez-Sanuy, F., Camargo-Ramírez, R., Gómez-Ariza, J., Baldrich, P., Campos-Soriano, L., Soto-Suárez, M., & San Segundo, B. (2021). A novel transposable element-derived microRNA participates in plant immunity to rice blast disease. Plant Biotechnology Journal, 19, 1798–1811.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Baulies, J. L., Bresso, E. G., Goldy, C., Palatnik, J. F., & Schommer, C. (2022). Potent inhibition of TCP transcription factors by miR319 ensures proper root growth in Arabidopsis. Plant Molecular Biology, 108, 93–103.

    Article  CAS  PubMed  Google Scholar 

  55. Curaba, J., Singh, M. B., & Bhalla, P. L. (2014). miRNAs in the crosstalk between phytohormone signalling pathways. Journal of Experimental Botany, 65, 1425–1438.

    Article  CAS  PubMed  Google Scholar 

  56. Schommer, C., Palatnik, J. F., Aggarwal, P., Chételat, A., Cubas, P., Farmer, E. E., Nath, U., & Weigel, D. (2008). Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biology, 6, e230.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Zhang, X., Bao, Y., Shan, D., Wang, Z., Song, X., Wang, Z., Wang, J., He, L., Wu, L., Zhang, Z., & Niu, D. (2018). Magnaporthe oryzae induces the expression of a microRNA to suppress the immune response in rice. Plant Physiology, 177, 352–368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Nicaise, V., Roux, M., & Zipfel, C. (2009). Recent advances in PAMP-triggered immunity against bacteria: Pattern recognition receptors watch over and raise the alarm. Plant Physiology, 150, 1638–1647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Šečić, E., Kogel, K. H., & Ladera-Carmona, M. J. (2021). Biotic stress-associated microRNA families in plants. Journal of Plant Physiology, 263, 153451

    Article  PubMed  Google Scholar 

  60. Lu, Y. B., Yang, L. T., Qi, Y. P., Li, Y., Li, Z., Chen, Y. B., Huang, Z. R., & Chen, L. S. (2014). Identification of boron-deficiency-responsive microRNAs in Citrus sinensis roots by Illumina sequencing. BMC Plant Biology, 14, 1–16.

    Article  CAS  Google Scholar 

  61. Lu, S., Sun, Y. H., & Chiang, V. L. (2008). Stress-responsive microRNAs in Populus. The Plant Journal, 55, 131–151.

    Article  CAS  PubMed  Google Scholar 

  62. Peng, W., Song, N., Li, W., Yan, M., Huang, C., Yang, Y., Duan, K., Dai, L., & Wang, B. (2021). Integrated analysis of microRNA and target genes in Brachypodium distachyon infected by Magnaporthe oryzae by small RNA and degradome sequencing. Frontiers in Plant Science, 12, 742347.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Chandran, V., Wang, H., Gao, F., Cao, X. L., Chen, Y. P., Li, G. B., Zhu, Y., Yang, X. M., Zhang, L. L., Zhao, Z. X., & Zhao, J. H. (2019). miR396-OsGRFs module balances growth and rice blast disease-resistance. Frontiers in Plant Science, 9, 1999.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Gupta, A., Patil, M., Qamar, A., & Senthil-Kumar, M. (2020). ath-miR164c influences plant responses to the combined stress of drought and bacterial infection by regulating proline metabolism. Environmental and Experimental Botany, 172, 103998.

    Article  CAS  Google Scholar 

  65. Zhou, T., Cao, L., Hu, K., Yu, X., & Qu, S. (2023). miR164–NAC21/22 module regulates the resistance of Malus hupehensis against Alternaria alternata by controlling jasmonic acid signaling. Plant Science, 330, 111635.

    Article  CAS  PubMed  Google Scholar 

  66. Campos, C., Coito, J. L., Cardoso, H., Marques da Silva, J., Pereira, H. S., Viegas, W., & Nogales, A. (2023). Dynamic regulation of grapevine’s microRNAs in response to mycorrhizal symbiosis and high temperature. Plants, 12, 982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Feng, Q., Li, Y., Zhao, Z. X., & Wang, W. M. (2021). Contribution of small RNA pathway to interactions of rice with pathogens and insect pests. Rice, 14, 1–15.

    Article  Google Scholar 

  68. Tan, J., Wu, Y., Guo, J., Li, H., Zhu, L., Chen, R., He, G., & Du, B. (2020). A combined microRNA and transcriptome analyses illuminates the resistance response of rice against brown planthopper. BMC Genomics, 21, 1–17.

    Article  Google Scholar 

  69. Zhang, L. L., Huang, Y. Y., Zheng, Y. P., Liu, X. X., Zhou, S. X., Yang, X. M., Liu, S. L., Li, Y., Li, J. L., Zhao, S. L., & Wang, H. (2022). Osa-miR535 targets SQUAMOSA promoter binding protein-like 4 to regulate blast disease resistance in rice. The Plant Journal, 110, 166–178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Islam, W., Tauqeer, A., Waheed, A., & Zeng, F. (2022). MicroRNA mediated plant responses to nutrient stress. International Journal of Molecular Sciences, 23, 2562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Li, Y., Cao, X. L., Zhu, Y., Yang, X. M., Zhang, K. N., Xiao, Z. Y., Wang, H., Zhao, J. H., Zhang, L. L., Li, G. B., & Zheng, Y. P. (2019). Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases. New Phytologist, 222, 1507–1522.

    Article  CAS  PubMed  Google Scholar 

  72. Li, Y., Lu, Y. G., Shi, Y., Wu, L., Xu, Y. J., Huang, F., Guo, X. Y., Zhang, Y., Fan, J., Zhao, J. Q., & Zhang, H. Y. (2014). Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiology, 164, 1077–1092.

    Article  CAS  PubMed  Google Scholar 

  73. Ye, Z., Zeng, J., Long, L., Ye, L., & Zhang, G. (2021). Identification of microRNAs in response to low potassium stress in the shoots of Tibetan wild barley and cultivated. Current Plant Biology, 25, 100193.

    Article  CAS  Google Scholar 

  74. Quoc, N. B., Phuong, N. D. N., Trang, H. T. T., Phi, N. B., & Chau, N. N. B. (2019). Expression of osa-miR7695 against the blast fungus Magnaporthe oryzae in Vietnamese rice cultivars. European Journal of Plant Pathology, 155, 307–317.

    Article  CAS  Google Scholar 

  75. Salvador-Guirao, R., Hsing, Y.-I., & San Segundo, B. (2018). The polycistronic miR166k-166h positively regulates rice immunity via post-transcriptional control of EIN2. Frontiers in Plant Science, 9, 337.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Naveed, Z. A., Wei, X., Chen, J., Mubeen, H., & Ali, G. S. (2020). The PTI to ETI continuum in Phytophthora-plant interactions. Frontiers in Plant Science, 11, 593905.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Zhang, R., Zhang, S., Hao, W., Song, G., Li, Y., Li, W., Gao, J., Zheng, Y., & Li, G. (2019). Lineage-specific evolved microRNAs regulating NB-LRR defense genes in Triticeae. International Journal of Molecular Sciences, 20, 3128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Cheng, H., Liu, H., Deng, Y., Xiao, J., Li, X., & Wang, S. (2015). The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiology, 167, 1087–1099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Rama Devi, S. J. S., Vutharadhi, S., Mahesh, H., & Bandameedi, A. (2022). Modulation of WRKY transcription factors in plant biotic stress responses. In P. Shukla, A. Kumar, R. Kumar, & M. K. Pandey (Eds.), Molecular response and genetic engineering for stress in plants, Volume 2: Biotic stress (pp. 11-1–11-20). IOP Publishing.

    Chapter  Google Scholar 

  80. Wu, Z., Li, T., Cao, X., Zhang, D., & Teng, N. (2022). Lily WRKY factor LlWRKY22 promotes thermotolerance through autoactivation and activation of LlDREB2B. Horticulture Research, 9, 186. https://doi.org/10.1093/hr/uhac186

    Article  Google Scholar 

  81. Rajput, L. S., Aggarwal, S. K., Mehta, S., Kumar, S., Nataraj, V., Shivakumar, M., Maheshwari, H. S., Yadav, S., & Goswami, D. (2020). Role of WRKY transcription factor superfamily in plant disease management. In B. Giri & M. P. Sharma (Eds.), Plant stress biology (pp. 335–361). Springer.

    Chapter  Google Scholar 

  82. Bakshi, M., Sherameti, I., Meichsner, D., Thürich, J., Varma, A., Johri, A. K., Yeh, K. W., & Oelmüller, R. (2017). Piriformospora indica reprograms gene expression in Arabidopsis phosphate metabolism mutants but does not compensate for phosphate limitation. Frontiers in Microbiology, 8, 1262.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Tang, W., Wang, F., Chu, H., You, M., Lv, Q., Ji, W., Deng, X., Zhou, B., & Peng, D. (2023). WRKY transcription factors regulate phosphate uptake in plants. Environmental and Experimental Botany, 208, 105241.

    Article  CAS  Google Scholar 

  84. Huang, Y., Li, M. Y., Wu, P., Xu, Z. S., Que, F., Wang, F., & Xiong, A. S. (2016). Members of WRKY Group III transcription factors are important in TYLCV defense signaling pathway in tomato (Solanum lycopersicum). BMC Genomics, 17, 1–18.

    Article  Google Scholar 

  85. Baldrich, P., & San Segundo, B. (2016). MicroRNAs in rice innate immunity. Rice, 9, 1–9.

    Article  Google Scholar 

  86. Peris-Peris, C., Serra-Cardona, A., Sánchez-Sanuy, F., Campo, S., Ariño, J., & San Segundo, B. (2017). Two NRAMP6 isoforms function as iron and manganese transporters and contribute to disease resistance in rice. Molecular Plant-Microbe Interactions, 30, 385–398.

    Article  CAS  PubMed  Google Scholar 

  87. Campo, S., & San Segundo, B. (2020). Systemic induction of phosphatidylinositol-based signaling in leaves of arbuscular mycorrhizal rice plants. Scientific Reports, 10, 1–17.

    Article  Google Scholar 

  88. Campo, S., Martín-Cardoso, H., Olivé, M., Pla, E., Catala-Forner, M., Martínez-Eixarch, M., & San Segundo, B. (2020). Effect of root colonization by arbuscular mycorrhizal fungi on growth, productivity and blast resistance in rice. Rice, 13, 1–14.

    Article  Google Scholar 

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RY wrote the manuscript draft. WR prepared the final manuscript. All authors read and approved the manuscript.

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Correspondence to Wusirika Ramakrishna.

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Yadav, R., Ramakrishna, W. MicroRNAs Involved in Nutritional Regulation During Plant–Microbe Symbiotic and Pathogenic Interactions with Rice as a Model. Mol Biotechnol (2023). https://doi.org/10.1007/s12033-023-00822-y

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