Physiological and biochemical markers associated with root lignification and micronutrient uptake in wheat genotypes with contrasting resistance to Gaeumannomyces tritici

1. Tripathi, R. et al. Plant mineral nutrition and disease resistance: A significant linkage for sustainable crop protection. Frontiers in Plant Science, 3116 (2022).

2. Coomey, J. H., Sibout, R. & Hazen, S. P. Grass secondary cell walls, Brachypodium distachyon as a model for discovery. New Phytol. 227, 1649–1667 (2020).

   Google Scholar 

3. Kolkman, J. M., Moreta, D. E., Repka, A., Bradbury, P. & Nelson, R. J. Brown midrib mutant and genome-wide association analysis uncover lignin genes for disease resistance in maize. The Plant Genome 16, e20278 (2023).

   Google Scholar 

4. Pérez, C. D. P. et al. Boron, zinc and manganese suppress rust on coffee plants grown in a nutrient solution. Eur. J. Plant Pathol. 156, 727–738 (2020).

   Google Scholar 

5. Sánchez-Sanuy, F. et al. Iron induces resistance against the rice blast fungus Magnaporthe oryzae through potentiation of immune responses. Rice 15, 68 (2022).

   Google Scholar 

6. Bellincampi, D., Cervone, F. & Lionetti, V. Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions. Front. Plant Sci. 5, 228 (2014).

   Google Scholar 

7. Lahlali, R. et al. Cell wall biomolecular composition plays a potential role in the host type II resistance to Fusarium head blight in wheat. Front. Microbiol. 7, 910 (2016).

   Google Scholar 

8. Martins, D., Araújo, S. d. S., Rubiales, D. & Vaz Patto, M. C. Legume crops and biotrophic pathogen interactions: A continuous cross-talk of a multilayered array of defense mechanisms. Plants 9, 1460 (2020).

9. Saberi Riseh, R., Gholizadeh Vazvani, M., Taheri, A. & Kennedy, J. F. Pectin-associated immune responses in plant-microbe interactions: A review. Int. J. Biol. Macromolec. 132790 (2024).

10. Jian, Y. et al. How plants manage pathogen infection. EMBO Rep. 25, 31–44 (2024).

    Google Scholar 

11. Miedes, E., Vanholme, R., Boerjan, W. & Molina, A. The role of the secondary cell wall in plant resistance to pathogens. Front. Plant Sci. 5, 100584 (2014).

    Google Scholar 

12. Bratovcic, A. Antioxidant enzymes and their role in preventing cell damage. Acta Sci. Nutr. Health 4, 01–07 (2020).

    Google Scholar 

13. Freitas, C. D. et al. Class III plant peroxidases: From classification to physiological functions. Int. J. Biol. Macromol. 263, 130306 (2024).

    Google Scholar 

14. Khan, T. A., Hilal, B. & Fariduddin, Q. in Hydrogen Peroxide 90–100 (CRC Press).

15. Zhai, X. et al. Overexpression of the peroxidase gene ZmPRX1 increases maize seedling drought tolerance by promoting root development and lignification. The Crop Journal 12, 753–765 (2024).

    Google Scholar 

16. Zhang, F. et al. Maize peroxidase ZmPrx25 modulates apoplastic ROS homeostasis and promotes seed germination and growth under osmotic and drought stresses. Antioxidants 14, 1067 (2025).

    Google Scholar 

17. Timofeeva, T. A., Bubnova, A. N., Shagdarova, B. T., Varlamov, V. P. & Kamionskaya, A. M. Phenylalanine ammonia-lyase-mediated differential response of tomato (Solanum lycopersicum L.) cultivars with different stress tolerance to treatment with low-molecular-weight chitosan. Agronomy 14, 386 (2024).

18. Lee, S. K. et al. Wild mungbean resistance to the nematode Meloidogyne enterolobii involves the induction of phenylpropanoid metabolism and lignification. Physiol. Plant. 176, e14533 (2024).

    Google Scholar 

19. Liu, X. et al. Transgenic wheat expressing Thinopyrum intermedium MYB transcription factor TiMYB2R-1 shows enhanced resistance to the take-all disease. J. Exp. Bot. 64, 2243–2253 (2013).

    Google Scholar 

20. Palma-Guerrero, J. et al. Take-all disease: new insights into an important wheat root pathogen. Trends Plant Sci. 26, 836–848 (2021).

    Google Scholar 

21. Rengel, Z., Graham, R. D. & Pedler, J. F. Time-course of biosynthesis of phenolics and lignin in roots of wheat genotypes differing in manganese efficiency and resistance to take-all fungus. Ann. Bot. 74, 471–477 (1994).

    Google Scholar 

22. Quiroz-Figueroa, F. R. et al. Cell wall-related genes and lignin accumulation contribute to the root resistance in different maize (Zea mays L.) genotypes to Fusarium verticillioides (Sacc.) nirenberg infection. Front. Plant Sci. 14, 1195794 (2023).

23. Dordas, C. Role of nutrients in controlling plant diseases in sustainable agriculture. A Review. Agronomy Sustain. Devel. 28, 33–46 (2008).

    Google Scholar 

24. Gholizadeh Vazvani, M., Dashti, H., Saberi Riseh, R. & Bihamta, M. R. Screening bread wheat germplasm for resistance to take-all disease (Gaeumannomyces graminis var. tritici) in greenhouse conditions. (2017).

25. Saberi Riseh, R., Dashti, H., Gholizadeh Vazvani, M. & Dini, A. Changes in the activity of enzymes phenylalanine ammonia-lyase, polyphenol oxidase, and peroxidase in some wheat genotypes against take-all disease. Journal of Agricultural Science and Technology 23, 929–942 (2021).

26. Freeman, J., Ward, E., Gutteridge, R. & Bateman, G. L. Methods for studying population structure, including sensitivity to the fungicide silthiofam, of the cereal take-all fungus Gaeumannomyces Graminis var. tritici. Plant Pathol. 54, 686–698 (2005).

    Google Scholar 

27. Doyle, J. in Molecular techniques in taxonomy 283–293 (Springer, 1991).

28. Gholizadah Vazvani, M., Dashti, H., Saberi Riseh, R. & Loit, E. Association analysis of response to take-all disease with agronomic traits and molecular markers and selection ideal genotypes in bread wheat (Triticum aestivum L.) genotypes. Molecul. Breed. https://doi.org/10.1007/s11032-025-01554-4 (2025).

29. Ownley, B. H., Duffy, B. K. & Weller, D. M. Identification and manipulation of soil properties to improve the biological control performance of phenazine-producing Pseudomonas fluorescens. Appl. Environ. Microbiol. 69, 3333–3343 (2003).

    Google Scholar 

30. Gholizadah Vazvani, M., Dashti, H., Saberi Riseh, R. & Bihamta, M. Screening Bread Wheat germplasm for resistance to take-all disease (Gaeumannomyces graminis var. tritici) in greenhouse conditions. J. Agricult. Sci. Techn. 19, 1173–1184 (2017).

31. Foster, C. E., Martin, T. M. & Pauly, M. Comprehensive compositional analysis of plant cell walls (lignocellulosic biomass) part I: lignin. JoVE J. Visualiz. Exper. e1745 (2010).

32. Fukushima, R. S. & Hatfield, R. D. Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J. Agric. Food Chem. 49, 3133–3139 (2001).

    Google Scholar 

33. Moreira-Vilar, F. C. et al. The acetyl bromide method is faster, simpler and presents best recovery of lignin in different herbaceous tissues than Klason and thioglycolic acid methods. PLoS ONE 9, e110000 (2014).

    Google Scholar 

34. Su, G., An, Z., Zhang, W. & Liu, Y. Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. J. Plant Physiol. 162, 1297–1303 (2005).

    Google Scholar 

35. Muhammad, A. et al. Survey of wheat straw stem characteristics for enhanced resistance to lodging. Cellulose 27, 2469–2484 (2020).

    Google Scholar 

36. Reddy, M., Tucker, M. R. & Dunn, S. Effect of manganese on concentrations of Zn, Fe, Cu and B in different soybean genotypes. Plant Soil 97, 57–62 (1987).

    Google Scholar 

37. Chapman, B., Jones, D. & Jung, R. F. Processes controlling metal ion attenuation in acid mine drainage streams. Geochim. Cosmochim. Acta 47, 1957–1973 (1983).

    Google Scholar 

38. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

    Google Scholar 

39. D’Cunha, G. B., Satyanarayan, V. & Nair, P. M. Stabilization of phenylalanine ammonia lyase containing Rhodotorula glutinis cells for the continuous synthesis of L-phenylalanine methyl ester/96. Enzyme Microb. Technol. 19, 421–427 (1996).

    Google Scholar 

40. Plewa, M. J., Smith, S. R. & Wagner, E. D. Diethyldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutation Research/Fundamental Mole. Mech. Mutagen. 247, 57–64 (1991).

    Google Scholar 

41. Bhuiyan, N. H., Selvaraj, G., Wei, Y. & King, J. Role of lignification in plant defense. Plant Signal. Behav. 4, 158–159 (2009).

    Google Scholar 

42. Vance, C., Kirk, T. & Sherwood, R. Lignification as a mechanism of disease resistance. Annu. Rev. Phytopathol. 18, 259–288 (1980).

    Google Scholar 

43. Zhang, S. H., Yang, Q. & Ma, R. C. Erwinia carotovora ssp. carotovora infection induced “defense lignin” accumulation and lignin biosynthetic gene expression in Chinese cabbage (Brassica rapa L. ssp. pekinensis). J. Integrat. Plant Biol. 49, 993–1002 (2007).

44. Moura, J. C. M. S., Bonine, C. A. V., de Oliveira Fernandes Viana, J., Dornelas, M. C. & Mazzafera, P. Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integrat. Plant Biol. 52, 360–376 (2010).

45. Jannoey, P., Pongprasert, W., Lumyong, S., Roytrakul, S. & Nomura, M. Comparative proteomic analysis of two rice cultivars (‘Oryza sativa‘L.) contrasting in Brown Planthopper (BPH) stress resistance. Plant Omics 8 (2015).

46. Kärkönen, A. & Koutaniemi, S. Lignin biosynthesis studies in plant tissue cultures. J. Integr. Plant Biol. 52, 176–185 (2010).

    Google Scholar 

47. Bonello, P. & Blodgett, J. T. Pinus nigra–Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol. Mol. Plant Pathol. 63, 249–261 (2003).

    Google Scholar 

48. Menden, B., Kohlhoff, M. & Moerschbacher, B. M. Wheat cells accumulate a syringyl-rich lignin during the hypersensitive resistance response. Phytochemistry 68, 513–520 (2007).

    Google Scholar 

49. Agarwal, P. K., Shukla, P. S., Gupta, K. & Jha, B. Bioengineering for salinity tolerance in plants: State of the art. Mol. Biotechnol. 54, 102–123 (2013).

    Google Scholar 

50. Sharma, N. K. et al. MicroRNA397 regulates tolerance to drought and fungal infection by regulating lignin deposition in chickpea root. Plant, Cell Environ. 46, 3501–3517 (2023).

    Google Scholar 

51. Mafa, M. S., Rufetu, E., Alexander, O., Kemp, G. & Mohase, L. Cell-wall structural carbohydrates reinforcements are part of the defence mechanisms of wheat against Russian wheat aphid (Diuraphis noxia) infestation. Plant Physiol. Biochem. 179, 168–178 (2022).

    Google Scholar 

52. Liu, R. et al. Integrative analysis of the multi-omics reveals the stripe rust fungus resistance mechanism of the TaPAL in wheat. Front. Plant Sci. 14, 1174450 (2023).

    Google Scholar 

53. Yang, X. et al. Lignin synthesis pathway in response to Rhizoctonia solani Kühn infection in potato (Solanum tuberosum L.). Chem. Biol. Techn. Agricult. 11, 135 (2024).

54. Chen, Y. et al. Comparative analysis of Fusarium crown rot resistance in synthetic hexaploid wheats and their parental genotypes. BMC Genomics 24, 178 (2023).

    Google Scholar 

55. Saberi Riseh, R., Dashti, H. & Gholizadeh Vazvani, M. Association between agronomic traits and molecular markers with take-all disease severity in bread wheat Triticum aestivum. J. Crop Protect. 11, 39–59 (2022).

56. Expert, D., Franza, T. & Dellagi, A. Iron in plant–pathogen interactions. Molecular aspects of iron metabolism in pathogenic and symbiotic plant-microbe associations, 7–39 (2012).

57. Huber, D. M. & Jones, J. B. The role of magnesium in plant disease. Plant Soil 368, 73–85 (2013).

    Google Scholar 

58. McMillan, V. et al. Exploring the resilience of wheat crops grown in short rotations through minimising the build-up of an important soil-borne fungal pathogen. Sci. Rep. 8, 9550 (2018).

    Google Scholar 

59. Puga-Freitas, R. et al. Transcriptional profiling of wheat in response to take-all disease and mechanisms involved in earthworm’s biocontrol effect. Eur. J. Plant Pathol. 144, 155–165 (2016).

    Google Scholar 

60. McCay-Buis, T., Huber, D., Graham, R. D., Phillips, J. & Miskin, K. Manganese seed content and take-all of cereals. J. Plant Nutr. 18, 1711–1721 (1995).

    Google Scholar 

61. Perfileva, A. I. & Krutovsky, K. V. Manganese nanoparticles: Synthesis, mechanisms of influence on plant resistance to stress, and prospects for application in agricultural chemistry. J. Agric. Food Chem. 72, 7564–7585 (2024).

    Google Scholar 

62. Lee, M. H. et al. Lignin-based barrier restricts pathogens to the infection site and confers resistance in plants. EMBO J. 38, e101948 (2019).

    Google Scholar 

63. Vanholme, R., Demedts, B., Morreel, K., Ralph, J. & Boerjan, W. Lignin biosynthesis and structure. Plant Physiol. 153, 895–905 (2010).

    Google Scholar 

64. Graham, R. D. & Webb, M. J. Micronutrients and disease resistance and tolerance in plants. Micronutrients Agricult. 4, 329–370 (1991).

    Google Scholar 

65. Aznar, A., Chen, N. W., Thomine, S. & Dellagi, A. Immunity to plant pathogens and iron homeostasis. Plant Sci. 240, 90–97 (2015).

    Google Scholar 

66. Liu, Q. et al. Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387, 323–336 (2015).

    Google Scholar 

67. Cakmak, I. et al. Chapter 7-function of nutrients: Micronutrients. Marschner’s mineral nutrition of higher plants (2022).

68. Herlihy, J. H., Long, T. A. & McDowell, J. M. Iron homeostasis and plant immune responses: Recent insights and translational implications. J. Biol. Chem. 295, 13444–13457 (2020).

    Google Scholar 

69. Ober, E. S. et al. Wheat root systems as a breeding target for climate resilience. Theor. Appl. Genet. 134, 1645–1662 (2021).

    Google Scholar 

70. Lequeux, H., Hermans, C., Lutts, S. & Verbruggen, N. Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol. Biochem. 48, 673–682 (2010).

    Google Scholar 

71. Tripathi, R. et al. Plant mineral nutrition and disease resistance: A significant linkage for sustainable crop protection. Front. Plant Sci. 13, 883970 (2022).

    Google Scholar 

72. Sun, J., Xiao, S. & Xue, C. The tug-of-war on iron between plant and pathogen. Phytopathology Research 5, 61 (2023).

    Google Scholar 

73. Gholizadeh Vazvani, M., Saberi Riseh, R. & Dashti, H. Lignification and nutrients in wheat: key factors for resistance to take-all disease. Journal of Plant Pathology, 1–14 (2025).

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