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Pathogenesis-Related Proteins (PRs) with Enzyme Activity Activating Plant Defense Responses

dos Santos, Cristiane, Franco, Octávio Luiz·2023·Plants
DOI 10.3390/plants12112226PMC PMC10255391
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Abstract

Throughout evolution, plants have developed a highly complex defense system against different threats, including phytopathogens. Plant defense depends on constitutive and induced factors combined as defense mechanisms. These mechanisms involve a complex signaling network linking structural and biochemical defense. Antimicrobial and pathogenesis-related (PR) proteins are examples of this mechanism, which can accumulate extra- and intracellular space after infection. However, despite their name, some PR proteins are present at low levels even in healthy plant tissues. When they face a pathogen, these PRs can increase in abundance, acting as the first line of plant defense. Thus, PRs play a key role in early defense events, which can reduce the damage and mortality caused by pathogens. In this context, the present review will discuss defense response proteins, which have been identified as PRs, with enzymatic action, including constitutive enzymes, β-1,3 glucanase, chitinase, peroxidase and ribonucleases. From the technological perspective, we discuss the advances of the last decade applied to the study of these enzymes, which are important in the early events of higher plant defense against phytopathogens.

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Figure 1 Initial plant defense response in plant–pathogen interaction. At first, the pathogen is recognized on the plant cell wall surface. Then, the elicitors activate a signaling network, where defense genes are activated to produce PR proteins that accumulate and act in the degradation of the pathogenic cell (i.e., β-1,3-gluc and chit; the degradation products of these enzymes can also act as elicitors). The oxidative buster mediates the generation of ROS in an attempt to limit the spread of the pathogen. PRs (i.e., β-1,3-glucanases, chitinases, PRXs, PR10 together with Phyx) are able to induce a hypersensitivity response to prevent the spread of the pathogen to other tissues, releasing elicitors that induce the plant’s defense mechanism. PR10, RBPs and RIPs are also produced by the plant, mediating virus infection. NB-LRR and PR10 act together in gene defense induction. PRX, peroxidase; PRs, pathogen-related proteins; Chit, chitinase; ROS, reactive oxygen species; Phyx, phytoalexin; β-1,3-gluc, β-1,3-glucanases; Ethy, ethylene; JA, jasmonic acid; LRR-RLK, leucine-rich repeat receptor-like protein kinase; NB-LRR, nucleotide-binding and leucine-rich repeat; RBPs, RNA-binding proteins; RIPs, ribosome-inactivating proteins.
Figure 1 Initial plant defense response in plant–pathogen interaction. At first, the pathogen is recognized on the plant cell wall surface. Then, the elicitors activate a signaling network, where defense genes are activated to produce PR proteins that accumulate and act in the degradation of the pathogenic cell (i.e., β-1,3-gluc and chit; the degradation products of these enzymes can also act as elicitors). The oxidative buster mediates the generation of ROS in an attempt to limit the spread of the pathogen. PRs (i.e., β-1,3-glucanases, chitinases, PRXs, PR10 together with Phyx) are able to induce a hypersensitivity response to prevent the spread of the pathogen to other tissues, releasing elicitors that induce the plant’s defense mechanism. PR10, RBPs and RIPs are also produced by the plant, mediating virus infection. NB-LRR and PR10 act together in gene defense induction. PRX, peroxidase; PRs, pathogen-related proteins; Chit, chitinase; ROS, reactive oxygen species; Phyx, phytoalexin; β-1,3-gluc, β-1,3-glucanases; Ethy, ethylene; JA, jasmonic acid; LRR-RLK, leucine-rich repeat receptor-like protein kinase; NB-LRR, nucleotide-binding and leucine-rich repeat; RBPs, RNA-binding proteins; RIPs, ribosome-inactivating proteins.CC BY · PubMed Central

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Research works printed but not linked: 110

  1. Li, 2020, The Lifecycle of the Plant Immune System, CRC Crit. Rev. Plant Sci., 39, 72, 10.1080/07352689.2020.1757829 · DOI
  2. Nishad, 2020, Modulation of Plant Defense System in Response to Microbial Interactions, Front. Microbiol., 11, 1298, 10.3389/fmicb.2020.01298 · DOI
  3. Pieterse, 2014, Induced systemic resistance by beneficial microbes, Annu. Rev. Phytopathol., 52, 347, 10.1146/annurev-phyto-082712-102340 · DOI · Paper page
  4. Nguyen, Q.-M., Iswanto, A.B.B., Son, G.H., and Kim, S.H. (2021). Recent advances in effector-triggered immunity in plants: New pieces in the puzzle create a different paradigm. Int. J. Mol. Sci., 22. · DOI
  5. Yuan, 2021, PTI-ETI crosstalk: An integrative view of plant immunity, Curr. Opin. Plant Biol., 62, 102030, 10.1016/j.pbi.2021.102030 · DOI
  6. Freeman, B., and Beattie, G. (2008). An overview of plant defenses against pathogens and herbivores. Overv. Plant Def. · DOI
  7. Mhlongo, 2018, The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance, Front. Plant Sci., 9, 112, 10.3389/fpls.2018.00112 · DOI
  8. Souza, 2017, Defense-related proteins involved in sugarcane responses to biotic stress, Genet. Mol. Biol., 40, 360, 10.1590/1678-4685-gmb-2016-0057 · DOI
  9. Ali, 2018, Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance, Microbiol. Res., 212, 29, 10.1016/j.micres.2018.04.008 · DOI
  10. Finkina, 2017, Plant pathogenesis-related proteins PR-10 and PR-14 as components of innate immunity system and ubiquitous allergens, Curr. Med. Chem., 24, 1772, 10.2174/0929867323666161026154111 · DOI
  11. Akbudak, 2020, Pathogenesis related protein-1 (PR-1) genes in tomato (Solanum lycopersicum L.): Bioinformatics analyses and expression profiles in response to drought stress, Genomics, 112, 4089, 10.1016/j.ygeno.2020.07.004 · DOI
  12. Pejchar, 2022, Immunity functions of Arabidopsis pathogenesis-related 1 are coupled but not confined to its C-terminus processing and trafficking, Mol. Plant Pathol., 23, 664, 10.1111/mpp.13187 · DOI
  13. Venancio, 2022, Pathogenesis-related protein 1 (PR-1) genes in soybean: Genome-wide identification, structural analysis and expression profiling under multiple biotic and abiotic stresses, Gene, 809, 146013, 10.1016/j.gene.2021.146013 · DOI
  14. Lu, 2018, Molecular characterization and functional analysis of PR-1-like proteins identified from the wheat head blight fungus Fusarium graminearum, Phytopathology, 108, 510, 10.1094/PHYTO-08-17-0268-R · DOI
  15. Chandrasekaran, 2016, Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology, Mol. Plant Pathol., 17, 1140, 10.1111/mpp.12375 · DOI · Paper page
  16. Shaw, 2019, Interaction of a plant virus protein with the signature Cajal body protein coilin facilitates salicylic acid-mediated plant defence responses, New Phytol., 224, 439, 10.1111/nph.15994 · DOI
  17. Sung, 2021, PR1-mediated defence via C-terminal peptide release is targeted by a fungal pathogen effector, New Phytol., 229, 3467, 10.1111/nph.17128 · DOI
  18. Anisimova, O.K., Shchennikova, A.V., Kochieva, E.Z., and Filyushin, M.A. (2021). Pathogenesis-Related Genes of PR1, PR2, PR4, and PR5 Families Are Involved in the Response to Fusarium Infection in Garlic (Allium sativum L.). Int. J. Mol. Sci., 22. · DOI
  19. Boccardo, 2019, Expression of pathogenesis-related proteins in transplastomic tobacco plants confers resistance to filamentous pathogens under field trials, Sci. Rep., 9, 2791, 10.1038/s41598-019-39568-6 · DOI
  20. Enoki, 2016, Pathogenesis-related proteins in grape, Grape Wine Biotechnol., 43, 46
  21. Santos, 2019, Proteomic analysis and functional validation of a Brassica oleracea endochitinase involved in resistance to Xanthomonas campestris, Front. Plant Sci., 10, 414, 10.3389/fpls.2019.00414 · DOI
  22. Zhang, J., Wang, F., Liang, F., Zhang, Y., Ma, L., Wang, H., and Liu, D. (2018). Functional analysis of a pathogenesis-related thaumatin-like protein gene TaLr35PR5 from wheat induced by leaf rust fungus. BMC Plant Biol., 18. · DOI
  23. Bashir, M.A., Silvestri, C., Ahmad, T., Hafiz, I.A., Abbasi, N.A., Manzoor, A., Cristofori, V., and Rugini, E. (2020). Osmotin: A cationic protein leads to improve biotic and abiotic stress tolerance in plants. Plants, 9. · DOI
  24. Rodríguez-Sifuentes, L., Marszalek, J.E., Chuck-Hernández, C., and Serna-Saldívar, S.O. (2020). Legumes protease inhibitors as biopesticides and their defense mechanisms against biotic factors. Int. J. Mol. Sci., 21. · DOI
  25. Sudisha, J., Sharathchandra, R.G., Amruthesh, K.N., Kumar, A., and Shetty, H.S. (2012). Plant Defence: Biological Control, Springer.
  26. Irigoyen, 2020, Genome-wide analyses of cassava Pathogenesis-related (PR) gene families reveal core transcriptome responses to whitefly infestation, salicylic acid and jasmonic acid, BMC Genom., 21, 93, 10.1186/s12864-019-6443-1 · DOI
  27. Kim, 2020, Overexpression of swpa4 peroxidase enhances tolerance to hydrogen peroxide and high salinity-mediated oxidative stress in transgenic sweetpotato plants, Plant Biotechnol. Rep., 14, 301, 10.1007/s11816-020-00602-z · DOI
  28. Sellami, 2022, Peroxidase enzymes as green catalysts for bioremediation and biotechnological applications: A review, Sci. Total Environ., 806, 150500, 10.1016/j.scitotenv.2021.150500 · DOI · Paper page
  29. Wu, 2016, Overexpression of a pathogenesis-related protein 10 enhances biotic and abiotic stress tolerance in rice, Plant Pathol. J., 32, 552, 10.5423/PPJ.OA.06.2016.0141 · DOI
  30. Mahmoud, 2020, Enhancing Tomato Plant Resistance Against Tobacco Mosaic Virus Using Riboflavin, Arab Univ. J. Agric. Sci., 28, 1257
  31. Peng, 2017, A sugarcane pathogenesis-related protein, ScPR10, plays a positive role in defense responses under Sporisorium scitamineum, SrMV, SA, and MeJA stresses, Plant Cell Rep., 36, 1427, 10.1007/s00299-017-2166-4 · DOI
  32. Franco, 2006, Identification of a cowpea γ-thionin with bactericidal activity, FEBS J., 273, 3489, 10.1111/j.1742-4658.2006.05349.x · DOI · Paper page
  33. Zhang, 2021, Antimicrobial peptides: Mechanism of action, activity and clinical potential, Mil. Med. Res., 8, 48
  34. Li, 2021, Plant antimicrobial peptides: Structures, functions, and applications, Bot. Stud., 62, 5, 10.1186/s40529-021-00312-x · DOI
  35. Höng, K., Austerlitz, T., Bohlmann, T., and Bohlmann, H. (2021). The thionin family of antimicrobial peptides. PLoS ONE, 16. · DOI
  36. Scheurer, 2018, Interaction of Non-Specific Lipid-Transfer Proteins With Plant-Derived Lipids and Its Impact on Allergic Sensitization, Front. Immunol., 9, 1389, 10.3389/fimmu.2018.01389 · DOI
  37. Wang, 2021, A nonspecific lipid transfer protein, StLTP10, mediates resistance to Phytophthora infestans in potato, Mol. Plant Pathol., 22, 48, 10.1111/mpp.13007 · DOI
  38. Fleury, 2019, Comprehensive classification of the plant non-specific lipid transfer protein superfamily towards its sequence–structure–function analysis, PeerJ, 7, e7504, 10.7717/peerj.7504 · DOI
  39. Kaur, A., Pati, P.K., Pati, A.M., and Nagpal, A.K. (2020). Physico-chemical characterization and topological analysis of pathogenesis-related proteins from Arabidopsis thaliana and Oryza sativa using in-silico approaches. PLoS ONE, 15. · DOI
  40. Farvardin, A., González-Hernández, A.I., Llorens, E., García-Agustín, P., Scalschi, L., and Vicedo, B. (2020). The apoplast: A key player in plant survival. Antioxidants, 9. · DOI
  41. Okushima, 2000, Secreted proteins of tobacco cultured BY2 cells: Identification of a new member of pathogenesis-related proteins, Plant Mol. Biol., 42, 479, 10.1023/A:1006393326985 · DOI
  42. Custers, 2004, Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence, Plant J., 39, 147, 10.1111/j.1365-313X.2004.02117.x · DOI
  43. Sooriyaarachchi, 2011, Expression and β-glucan binding properties of Scots pine (Pinus sylvestris L.) antimicrobial protein (Sp-AMP), Plant Mol. Biol., 77, 33, 10.1007/s11103-011-9791-z · DOI
  44. Singh, A., and Singh, I.K. (2018). Molecular Aspects of Plant-Pathogen Interaction, Springer. · DOI
  45. Zribi, 2021, Pathogenesis Related Proteins (PRs): From Cellular Mechanisms to Plant Defense, Curr. Protein Pept. Sci., 22, 396, 10.2174/1389203721999201231212736 · DOI · Paper page
  46. Ali, 2021, The DNA–carbon nanotube binding mode determines the efficiency of carbon nanotube-mediated DNA delivery to intact plants, ACS Appl. Nano Mater., 5, 4663, 10.1021/acsanm.1c03482 · DOI
  47. Adrian, 2019, Recognition of Elicitors in Grapevine: From MAMP and DAMP Perception to Induced Resistance, Front. Plant Sci., 10, 1117, 10.3389/fpls.2019.01117 · DOI
  48. Jamiołkowska, A. (2020). Natural Compounds as Elicitors of Plant Resistance Against Diseases and New Biocontrol Strategies. Agronomy, 10. · DOI
  49. Wang, 2021, A novel β-1,3-glucanase Gns6 from rice possesses antifungal activity against Magnaporthe oryzae, J. Plant Physiol., 265, 153493, 10.1016/j.jplph.2021.153493 · DOI
  50. Stintzi, 1993, Plant ‘pathogenesis-related’proteins and their role in defense against pathogens, Biochimie, 75, 687, 10.1016/0300-9084(93)90100-7 · DOI
  51. Ding, 2022, Redesigning Enzymes for Biocatalysis: Exploiting Structural Understanding for Improved Selectivity, Front. Mol. Biosci., 9, 684, 10.3389/fmolb.2022.908285 · DOI
  52. Engqvist, 2019, Applications of protein engineering and directed evolution in plant research, Plant Physiol., 179, 907, 10.1104/pp.18.01534 · DOI
  53. Talavera-Caro, A.G., Alva-Sánchez, D.L., Sosa-Herrera, A., Sánchez-Muñoz, M.A., Hernández-De Lira, I.O., Hernández-Beltran, J.U., Hernández-Almanza, A.Y., and Balagurusamy, N. (2022). Value-Addition in Food Products and Processing Through Enzyme Technology, Elsevier Academic Press.
  54. Linton, 2020, The structure and function of cellulase (endo-β-1, 4-glucanase) and hemicellulase (β-1, 3-glucanase and endo-β-1, 4-mannase) enzymes in invertebrates that consume materials ranging from microbes, algae to leaf litter, Comp. Biochem. Physiol. Part B Biochem. Mol. Biol., 240, 110354, 10.1016/j.cbpb.2019.110354 · DOI
  55. Balasubramanian, 2012, Plant β-1, 3-glucanases: Their biological functions and transgenic expression against phytopathogenic fungi, Biotechnol. Lett., 34, 1983, 10.1007/s10529-012-1012-6 · DOI
  56. Geelen, 2014, Callose homeostasis at plasmodesmata: Molecular regulators and developmental relevance, Front. Plant Sci., 5, 138
  57. Russell, 2019, Barley grain (1, 3; 1, 4)-β-glucan content: Effects of transcript and sequence variation in genes encoding the corresponding synthase and endohydrolase enzymes, Sci. Rep., 9, 17250, 10.1038/s41598-019-53798-8 · DOI
  58. Perrot, T., Pauly, M., and Ramírez, V. (2022). Emerging Roles of β-Glucanases in Plant Development and Adaptative Responses. Plants, 11. · DOI · Paper page
  59. Paniagua, C., Perry, L., and Benitez-Alfonso, Y. (2021). A phylogenetic and transcriptomic study of the β-1, 3-glucanase family in tomato identifies candidate targets for fruit improvement. bioRxiv. · DOI
  60. Wu, Q., Dou, X., Wang, Q., Guan, Z., Cai, Y., and Liao, X. (2018). Isolation of β-1,3-Glucanase-Producing Microorganisms from Poria cocos Cultivation Soil via Molecular Biology. Molecules, 23. · DOI
  61. Pusztahelyi, 2018, Chitin and chitin-related compounds in plant–fungal interactions, Mycology, 9, 189, 10.1080/21501203.2018.1473299 · DOI
  62. Wanke, 2021, Unraveling the sugar code: The role of microbial extracellular glycans in plant–microbe interactions, J. Exp. Bot., 72, 15, 10.1093/jxb/eraa414 · DOI
  63. Xu, J., Zhang, N., Wang, K., Xian, Q., Dong, J., Qi, X., and Chen, X. (2022). Chitinase Chi 2 Positively Regulates Cucumber Resistance against Fusarium oxysporum f. sp. cucumerinum. Genes, 13. · DOI
  64. Liu, 2020, A Na2CO3-Responsive Chitinase Gene From Leymus chinensis Improve Pathogen Resistance and Saline-Alkali Stress Tolerance in Transgenic Tobacco and Maize, Front. Plant Sci., 11, 1
  65. Xin, Y., Wang, D., Han, S., Li, S., Gong, N., Fan, Y., and Ji, X. (2021). Characterization of the chitinase gene family in mulberry (Morus notabilis) and MnChi18 involved in resistance to Botrytis cinerea. Genes, 13. · DOI
  66. Ali, M., Li, Q.H., Zou, T., Wei, A.M., Gombojab, G., Lu, G., and Gong, Z.H. (2020). Chitinase Gene Positively Regulates Hypersensitive and Defense Responses of Pepper to Colletotrichum acutatum Infection. Int. J. Mol. Sci., 21. · DOI
  67. Franzener, 2018, Induction of defense enzymes and control of anthracnose in cucumber by Corymbia citriodora aqueous extract, Summa Phytopathol., 44, 10, 10.1590/0100-5405/2218 · DOI
  68. Oliveira, 2016, Induced resistance during the interaction pathogen x plant and the use of resistance inducers, Phytochem. Lett., 15, 152, 10.1016/j.phytol.2015.12.011 · DOI
  69. Choudhary, 2020, ROS and oxidative burst: Roots in plant development, Plant Divers., 42, 33, 10.1016/j.pld.2019.10.002 · DOI
  70. Sorokan, 2018, Anionic peroxidase-mediated oxidative burst requirement for jasmonic acid-dependent Solanum tuberosum defence against Phytophthora infestans, Plant Pathol., 67, 349, 10.1111/ppa.12743 · DOI
  71. Bela, K., Riyazuddin, R., and Csiszár, J. (2022). Plant Glutathione Peroxidases: Non-Heme Peroxidases with Large Functional Flexibility as a Core Component of ROS-Processing Mechanisms and Signalling. Antioxidants, 11. · DOI
  72. Twala, 2020, Breakthroughs in the discovery and use of different peroxidase isoforms of microbial origin, AIMS Microbiol., 6, 330, 10.3934/microbiol.2020020 · DOI
  73. Kaur, 2022, How do plants defend themselves against pathogens-Biochemical mechanisms and genetic interventions, Physiol. Mol. Biol. Plants, 28, 485, 10.1007/s12298-022-01146-y · DOI
  74. Blaschek, 2021, Phenoloxidases in plants—How structural diversity enables functional specificity, Front. Plant Sci., 12, 754601, 10.3389/fpls.2021.754601 · DOI
  75. Campos, 2004, Peroxidase and polyphenol oxidase activity in bean anthracnose resistance, Pesqui. Agropecu. Bras., 39, 637, 10.1590/S0100-204X2004000700004 · DOI
  76. Basumatary, 2023, The role of peroxidases in the bioremediation of organic pollutants, Nat. Prod. J., 13, 60
  77. Kurnik, 2015, Removal of phenol from synthetic and industrial wastewater by potato pulp peroxidases, Water Air Soil Pollut., 226, 254, 10.1007/s11270-015-2517-0 · DOI
  78. Lakshmi, 2018, Characterization of peroxidase enzyme and detoxification of phenols using peroxidase enzyme obtained from Zea mays L waste, Appl. Water Sci., 8, 207, 10.1007/s13201-018-0820-9 · DOI
  79. Zechmann, B. (2020). Subcellular Roles of Glutathione in Mediating Plant Defense during Biotic Stress. Plants, 9. · DOI
  80. Hasanuzzaman, M., Nahar, K., Hossain, M.S., Mahmud, J.A., Rahman, A., Inafuku, M., Oku, H., and Fujita, M. (2017). Coordinated Actions of Glyoxalase and Antioxidant Defense Systems in Conferring Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci., 18. · DOI
  81. Gullner, 2019, Contribution of cell wall peroxidase-and NADPH oxidase-derived reactive oxygen species to Alternaria brassicicola-induced oxidative burst in Arabidopsis, Mol. Plant Pathol., 20, 485, 10.1111/mpp.12769 · DOI
  82. Zhao, 2019, A class III peroxidase PRX34 is a component of disease resistance in Arabidopsis, J. Gen. Plant Pathol., 85, 405, 10.1007/s10327-019-00863-9 · DOI
  83. Carmo, 2022, Overexpression of cotton genes GhDIR4 and GhPRXIIB in Arabidopsis thaliana improves plant resistance to root-knot nematode (Meloidogyne incognita) infection, 3 Biotech, 12, 211
  84. Do, 2022, Development of a genome-edited tomato with high ascorbate content during later stage of fruit ripening through mutation of SlAPX4, Front. Plant Sci., 13, 1, 10.3389/fpls.2022.836916 · DOI
  85. Pandey, 2017, Abiotic stress tolerance in plants: Myriad roles of ascorbate peroxidase, Front. Plant Sci., 8, 581, 10.3389/fpls.2017.00581 · DOI
  86. Wu, B., and Wang, B. (2019). Comparative analysis of ascorbate peroxidases (APXs) from selected plants with a special focus on Oryza sativa employing public databases. PLoS ONE, 14. · DOI
  87. Akram, 2017, Ascorbic acid-a potential oxidant scavenger and its role in plant development and abiotic stress tolerance, Front. Plant Sci., 8, 613, 10.3389/fpls.2017.00613 · DOI
  88. Chin, 2019, Plant cytosolic ascorbate peroxidase with dual catalytic activity modulates abiotic stress tolerances, Iscience, 16, 31, 10.1016/j.isci.2019.05.014 · DOI
  89. Riyazuddin, R., Bela, K., Poór, P., Szepesi, Á., Horváth, E., Rigó, G., Szabados, L., Fehér, A., and Csiszár, J. (2022). Crosstalk between the Arabidopsis glutathione peroxidase-like 5 Isoenzyme (AtGPXL5) and ethylene. Int. J. Mol. Sci., 23. · DOI
  90. Li, 2020, CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification, Hortic. Res., 7, 192, 10.1038/s41438-020-00415-9 · DOI
  91. Kuo, 2020, Ascorbate peroxidase 4 plays a role in the tolerance of Chlamydomonas reinhardtii to photo-oxidative stress, Sci. Rep., 10, 13287, 10.1038/s41598-020-70247-z · DOI
  92. Aglas, 2020, Ligand binding of PR-10 proteins with a particular focus on the Bet v 1 allergen family, Curr. Allergy Asthma Rep., 20, 25, 10.1007/s11882-020-00918-4 · DOI · Paper page
  93. Ghorbel, 2021, Differential regulation of the durum wheat Pathogenesis-related protein (PR1) by Calmodulin TdCaM1. 3 protein, Mol. Biol. Rep., 48, 347, 10.1007/s11033-020-06053-7 · DOI
  94. Longsaward, R., Pengnoo, A., Kongsawadworakul, P., and Viboonjun, U. (2023). A novel rubber tree PR-10 protein involved in host-defense response against the white root rot fungus Rigidoporus microporus. BMC Plant Biol., 23. · DOI
  95. Zarattini, 2017, The bile acid deoxycholate elicits defences in Arabidopsis and reduces bacterial infection, Mol. Plant Pathol., 18, 540, 10.1111/mpp.12416 · DOI
  96. Besbes, F., Habegger, R., and Schwab, W. (2019). Induction of PR-10 genes and metabolites in strawberry plants in response to Verticillium dahliae infection. BMC Plant Biol., 19. · DOI
  97. Genzel, 2018, Systemic induction of salicylic acid-related plant defences in potato in response to Rhizoctonia solani AG 3 PT, Plant Pathol., 67, 337, 10.1111/ppa.12746 · DOI
  98. Besbes, 2019, Phosphorylation-dependent ribonuclease activity of Fra a 1 proteins, J. Plant Physiol., 233, 1, 10.1016/j.jplph.2018.12.002 · DOI
  99. Huh, 2013, Plant RNA binding proteins for control of RNA virus infection, Front. Physiol., 4, 397, 10.3389/fphys.2013.00397 · DOI
  100. Islam, M.M., Qi, S., Zhang, S., Amin, B., Yadav, V., El-Sappah, A.H., Zhang, F., and Liang, Y. (2022). Genome-Wide Identification and Functions against Tomato Spotted Wilt Tospovirus of PR-10 in Solanum lycopersicum. Int. J. Mol. Sci., 23. · DOI
  101. Wieczorek, 2019, Contribution of Tomato torrado virus Vp26 coat protein subunit to systemic necrosis induction and virus infectivity in Solanum lycopersicum, Virol. J., 16, 9, 10.1186/s12985-019-1117-9 · DOI
  102. Sinha, 2020, Role of Pathogen-Related Protein 10 (PR 10) under abiotic and biotic stresses in plants, Phyton, 89, 167, 10.32604/phyton.2020.09359 · DOI
  103. McBride, J.K., Cheng, H., Maleki, S.J., and Hurlburt, B.K. (2019). Purification and characterization of pathogenesis related class 10 panallergens. Foods, 8. · DOI
  104. Choi, 2012, Requirement of the cytosolic interaction between pathogenesis-related protein 10 and leucine-rich repear protein 1 for cell death and defense signaling in pepper, Plant Cell, 24, 1675, 10.1105/tpc.112.095869 · DOI
  105. Lee, 2012, Expression and stress tolerance of PR10 genes from Panax ginseng C. A. Meyer, Mol. Biol. Rep., 39, 2365, 10.1007/s11033-011-0987-8 · DOI
  106. Andrade, 2010, Effects of a novel pathogenesis-related class 10 (PR-10) protein from crotalaria pallida roots with papain inhibitory activity against root-knot nematode Meloidogyne incognita, J. Agric. Food Chem., 58, 4145, 10.1021/jf9044556 · DOI
  107. Li, 2021, Diversified regulation of cytokinin levels and signaling during Botrytis cinerea infection in Arabidopsis, Front. Plant Sci., 12, 584042, 10.3389/fpls.2021.584042 · DOI
  108. Gao, 2019, Structure Analysis of a Pathogenesis-Related 10 Protein from Gardenia jasminoides, IOP Conf. Ser. Earth Environ. Sci., 2019, 042005, 10.1088/1755-1315/242/4/042005 · DOI
  109. Wang, 2021, A Valsa mali Effector Protein 1 Targets Apple (Malus domestica) Pathogenesis-Related 10 Protein to Promote Virulence, Front. Plant Sci., 12, 1
  110. Romera, 2019, Induced Systemic Resistance (ISR) and Fe Deficiency Responses in Dicot Plants, Front. Plant Sci., 10, 287, 10.3389/fpls.2019.00287 · DOI

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Metadata

Authors
dos Santos, C., & Franco, O. L.
Venue
Plants
Publisher
MDPI AG
Published
2023-06-05
Volume
12
Issue
11
Pages
2226
ISSN
2223-7747
DOI
10.3390/plants12112226
PMC
PMC10255391
Cited by
259
References
0
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Pathogenesis-Related Proteins (PRs) with Enzyme Activity Activating Plant Defense Responses. https://app.cochat.ai/papers/10.3390/plants12112226
The paper
dos Santos, C., & Franco, O. L. (2023). Pathogenesis-Related Proteins (PRs) with Enzyme Activity Activating Plant Defense Responses. Plants. https://doi.org/10.3390/plants12112226