Tryptic Digested Protein Transglutaminase Elicitor Can Improve Plant Physiological Parameters: A Computational Approach to Insight Molecular Interactions
Keywords:
Transglutaminase activity, Structural analysis, Pathogenicity protein, Functional annotation, TgaseAbstract
Phytophthora melonis causes horticultural crops' dieback, foot rot, root rot, crown rot, and blight. It possesses multiple pathogenicity factors, and transglutaminase is among the most effective pathogenicity tools of Phytophthora. We have isolated the pathogenic enzyme and applied its tryptically digested fragments to tomato plants to exploit effector proteins for the augmentation of plant defenses, physiological parameters, antioxidative machinery, and evapotranspiration. The results revealed that the treatment significantly increased agronomic traits, e.g., root length, shoot length, root biomass, shoot biomass, root dry mass, shoot dry mass, and leaf area, around 30% in each case. Furthermore, an increase of more than 10% was observed in the case of photosynthetic parameters. At the same time, the antioxidative machinery (enzymatic and biochemical) was more than 53% more efficient than the control plants. Similarly, the evapotranspiration and electrolyte leakage improved by more than 18%. Furthermore, the pathogenic enzyme underwent structural and functional characterization. The biochemical tolerance tests revealed the temperature of 37 °C and pH of 6.4 as the optimum circumstances of the enzyme. The Tween-80 application increased activity by 136.72%, although higher temperatures reduced the stability of the enzyme. The structural protein annotations exhibited 2 monomers, including A (260-620) and B (141-219). Elicitation of transglutaminase (TGase) and antifreeze attributes were revealed by monomer A and monomer B, respectively. Additionally, an association of 6 ligand molecules of 3-cyclohexyl-1-propylsulfonic acidic were observed to maintain the enzymatic activity. Overall, the protein was categorized as the freeze-resistant protein that was revealed in three genera, i.e., Plasmopara, Phytophthora, and Pythium, according to the biome distribution analysis. Whereas the protein was also present in some other taxonomic classes (i.e., archaea, and bacteria). The current study is a new approach to exploit the plant metabolic machinery for improved cellular defenses and metabolism. It will also help to interpret the supramolecular interactions between the pathogen and its host, especially in a pathogen from oomycetes.
References
Ahmad A, Shafique S, Shafique S. Cytological and physiological basis for tomato varietal resistance against Alternaria alternata. J Sci Food Agric 2013;93(9):2315-22.
Ahmad A, Khan WU, Shah AA, Yasin NA, Ali A, Rizwan M, Ali S. Dopamine Alleviates Hydrocarbon Stress in Brassica oleracea through Modulation of Physio-Biochemical Attributes and Antioxidant Defense Systems. Chemosphere 2021a;270:128633.
Ahmad A, Akram W, Shahzadi I, Wang R, Hu D, Li G, Yasin NA, Ahmed S, Wu T. First Report of Fusarium nelsonii Causing Early-Stage Fruit Blight of Cucumber in Guangzhou, China. Plant Disease 2020a;104(5).
Ahmad A, Akram W, Bashir Z, Shahzadi I, Wang R, Abbas HMK, Hu D, Ahmed S, Xu X, Li G, Wu T. Functional and Structural Analysis of a Novel Acyltransferase from Pathogenic Phytophthora melonis. ACS Omega 2021b;6(3):1797-1808.
Ahmad A, Khan TA, Mubeen S, Shahzadi I, Akram W, Saeed T, Bashir Z, Wang R, Alam M, Ahmed S, Hu D, Li G, Wu T. Metabolic and Proteomic Perspectives of Augmentation of Nutritional Contents and Plant Defense in Vigna unguiculata. Biomolecules 2020b;10(2).
Ahmad HI, Ahmad MJ, Asif AR, Adnan M, Iqbal MK, Mehmood K, Muhammad SA, Bhuiyan AA, Elokil A, Du X, Zhao C, Liu X, Xie S. A Review of CRISPR-Based Genome Editing: Survival, Evolution and Challenges. Curr Issues Mol Biol 2018;28:47-68.
Ahmad HI, Asif AR, Ahmad MJ, Jabbir F, Adnan M, Ahmed S, Afzal G, Saleem AH, Li L, Jiang H, Simirgiotis MJ, Rauf M, Chen J. Adaptive evolution of peptidoglycan recognition protein family regulates the innate signaling against microbial pathogens in vertebrates. Microbial Pathogenesis 2020c;147.
Akram W, Anjum T, Ahmad A. Basal susceptibility of tomato varieties against different isolates of fusarium oxysporum f. sp. lycopersici. International Journal of Agriculture and Biology 2014;16(1):171-176.
Akram W, Anjum T, Ali B, Ahmad A. Screening of native bacillus strains to induce systemic resistance in tomato plants against fusarium wilt in split root system and its field applications. International Journal of Agriculture and Biology 2013;15(6).
Ali S, Zhu Q, Jaleel W, Rehman SU, Rasheed MA, Khan MM, Islam Y, Hafeez M, Zhou X. Determination of fitness traits of Orius strigicollis Poppius (Hemiptera: Anthocoridae) on Pectinophora gossypiella (Lepidoptera: Gelechiidae) using two-sex life table analysis. PeerJ 2020;8:e9594.
Bashir Z, Shafique S, Ahmad A, Shafique S, Yasin NA, Ashraf Y, Ibrahim A, Akram W, Noreen S. Tomato Plant Proteins Actively Responding to Fungal Applications and Their Role in Cell Physiology. Front Physiol 2016;7:257.
Cline ET, Farr DF, Rossman AY. A Synopsis of Phytophthora with Accurate Scientific Names, Host Range, and Geographic Distribution. Plant Health Progress 2008;9(1):32-32.
Dai Z, Edwards GE, Ku MS. Control of Photosynthesis and Stomatal Conductance in Ricinus communis L. (Castor Bean) by Leaf to Air Vapor Pressure Deficit. Plant Physiol 1992;99(4):1426-34.
Garner ALJanda KD. cat-ELCCA: a robust method to monitor the fatty acid acyltransferase activity of ghrelin O-acyltransferase (GOAT). Angew Chem Int Ed Engl 2010;49(50):9630-4.
Greene NP, Crow A, Hughes C, Koronakis V. Structure of a bacterial toxin-activating acyltransferase. Proceedings of the National Academy of Sciences 2015;112(23):E3058-66.
Hafeez M, Qasim M, Ali S, Yousaf HK, Waqas M, Ali E, Ahmad MA, Jan S, Bashir MA, Noman A, Wang M, Gharmh HA, Khan KA. Expression and functional analysis of P450 gene induced tolerance/resistance to lambda-cyhalothrin in quercetin fed larvae of beet armyworm Spodoptera exigua (Hubner). Saudi Journal of Biological Sciences 2020;27(1):77-87.
Han Z, Gao H, Ye L, Adil MF, Ahsan M, Zhang G. Identification of QTLs associated with p-coumaric acid and ferulic acid in barley. Euphytica 2019;215(12):198-198.
Hashemi L, Golparvar AR, Nasr Esfahani M, Golabadi M. Correlation between cucumber genotype and resistance to damping-off disease caused by Phytophthora melonis. Biotechnology & Biotechnological Equipment 2019;33(1):1494-1504.
Ibrahim A, Shahid AA, Ahmad A. Evaluation of carrier materials to develop Bacillus subtilis formulation to control root knot nematode infection and promote agroeconomic traits in eggplant. Journal of Animal and Plant Sciences 2017;27(4):1321-1330.
Ibrahim A, Shahid AAAA, Noreen S, Ahmad A. Physiological changes against meloidogyne incognita in rhizobacterial treated eggplant under organic conditions. Journal of Animal and Plant Sciences 2016;26(3):805-813.
Javaid A, Akram W, Shoaib A, Haider MS, Ahmad A. ISSR analysis of genetic diversity in Dalbergia sissoo in Punjab, Pakistan. Pakistan Journal of Botany 2014;46(5):1573-1576.
Khan TA, Yusuf M, Ahmad A, Bashir Z, Saeed T, Fariduddin Q, Hayat S, Mock HP, Wu T. Proteomic and physiological assessment of stress sensitive and tolerant variety of tomato treated with brassinosteroids and hydrogen peroxide under low-temperature stress. Food Chem 2019;289(March):500-511.
Khan WU, Yasin NA, Ahmad SR, Ali A, Ahmad A, Akram W, Faisal M. Role of Burkholderia cepacia CS8 in Cd-stress alleviation and phytoremediation by Catharanthus roseus. Int J Phytoremediation 2018;20(6):581-592.
Konishi T, Kato K, Araki T, Shiraki K, Takagi M, Tamaru Y. A new class of glutathione S-transferase from the hepatopancreas of the red sea bream Pagrus major. Biochem J 2005;388(Pt 1):299-307.
Lee Y-H, Severino V, Farina A, Fleischmann F, Dalio RJD, Di Maro A, Scognamiglio M, Fiorentino A, Parente A, Osswald W, Chambery A. Molecular Profiling of the Phytophthora plurivora Secretome: A Step towards Understanding the Cross-Talk between Plant Pathogenic Oomycetes and Their Hosts. PLoS ONE 2014;9(11):e112317-e112317.
Li G, Shah AA, Khan WU, Yasin NA, Ahmad A, Abbas M, Ali A, Safdar N. Hydrogen sulfide mitigates cadmium induced toxicity in Brassica rapa by modulating physiochemical attributes, osmolyte metabolism and antioxidative machinery. Chemosphere 2021;263:127999.
Li Q, Hu L, Guo J, Yang T, Chen L. Molecular characterization of two type I acyl-CoA: diacylglycerol acyltransferase genes in maize. Biotechnology & Biotechnological Equipment 2016;30(3):453-461.
Liu J, Shi J, Li J, Yuan X. Effects of surfactants tween 80 and rhamnolipid on the extracellular enzymes amylase, protease, CMCase and xylanase of one strain. Proceedings - International Conference on Computer Distributed Control and Intelligent Environmental Monitoring, CDCIEM 20112011. p. 1207-1210.
Lwalaba JLW, Zvobgo G, Gai Y, Issaka JH, Mwamba TM, Louis LT, Fu L, Nazir MM, Ansey Kirika B, Kazadi Tshibangu A, Adil MF, Sehar S, Mukobo RP, Zhang G. Transcriptome analysis reveals the tolerant mechanisms to cobalt and copper in barley. Ecotoxicology and Environmental Safety 2021;209:111761.
Mapodzeke JM, Adil MF, Wei D, Joan HI, Ouyang Y, Shamsi IH. Modulation of Key Physio-Biochemical and Ultrastructural Attributes after Synergistic Application of Zinc and Silicon on Rice under Cadmium Stress. Plants (Basel) 2021;10(1):87-87.
McFie PJStone SJ. A fluorescent assay to quantitatively measure in vitro acyl CoA:diacylglycerol acyltransferase activity. J Lipid Res 2011;52(9):1760-4.
Ogawa T, Tanaka A, Kawamoto J, Kurihara T. Purification and characterization of 1-acyl-sn-glycerol-3-phosphate acyltransferase with a substrate preference for polyunsaturated fatty acyl donors from the eicosapentaenoic acid-producing bacterium Shewanella livingstonensis Ac10. J Biochem 2018;164(1):33-39.
Payehghadr M, Esmaeilpour S, Kazem Rofouei M, Adlnasab L, Mourran A. Determination of Trace Amount of Cadmium by Atomic Absorption Spectrometry in Table Salt after Solid Phase Preconcentration Using Octadecyl Silica Membrane Disk Modified by a New Derivative of Pyridine. Journal of Chemistry 2012;2013(1).
Reiss K, Kirchner E, Gijzen M, Zocher G, Loffelhardt B, Nurnberger T, Stehle T, Brunner F. Structural and phylogenetic analyses of the GP42 transglutaminase from Phytophthora sojae reveal an evolutionary relationship between oomycetes and marine Vibrio bacteria. J Biol Chem 2011;286(49):42585-42593.
Shafique S, Ahmad A, Shafique S, Anjum T, Akram W, Bashir Z. Determination of Molecular and Biochemical Changes in Cotton Plants Mediated by Mealybug. NJAS: Wageningen Journal of Life Sciences 2022;70-71(1):39-45.
Shahzadi I, Khan ZH, Akram W, Khan WU, Ahmad A, Yasin NA, Yujie L. Heavy metal and organic pollutants removal from water using bilayered polydopamine composite of sandwiched graphene Nanosheets: One solution for two obstacles. Separation and Purification Technology 2022;280.
Sharma M, Guleria S, Kulshrestha S. Diacylglycerol acyl transferase: A pathogenicity related gene in Colletotrichum gloeosporioides. J Basic Microbiol 2016;56(11):1308-1315.
Shi Y, Wang Q, Hou Y, Hong Y, Han X, Yi J, Qu J, Lu Y. Molecular cloning, expression and enzymatic characterization of glutathione S-transferase from Antarctic sea-ice bacteria Pseudoalteromonas sp. ANT506. Microbiol Res 2014;169(2-3):179-84.
Siddiqui JA, Bamisile BS, Khan MM, Islam W, Hafeez M, Bodlah I, Xu Y. Impact of invasive ant species on native fauna across similar habitats under global environmental changes. Environmental science and pollution research international 2021;28(39):54362-54382.
Tariq M, Shah AA, Yasin NA, Ahmad A, Rizwan M. Enhanced performance of Bacillus megaterium OSR-3 in combination with putrescine ammeliorated hydrocarbon stress in Nicotiana tabacum. Int J Phytoremediation 2021;23(2):119-129.
Thompson SE, Levin S, Rodriguez-Iturbe I. Rainfall and temperatures changes have confounding impacts on Phytophthora cinnamomi occurrence risk in the southwestern USA under climate change scenarios. Glob Chang Biol 2014;20(4):1299-312.
Tingquan W. Stability determination of candidate reference genes in cucumber plants subjected to stresses from Phytophthora melonis. Journal of Plant Science and Phytopathology 2019;3(1):028-035.
Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CM, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour KH, Lee MK, McDonald WH, Medina M, Meijer HJ, Nordberg EK, Maclean DJ, Ospina-Giraldo MD, Morris PF, Phuntumart V, Putnam NH, Rash S, Rose JK, Sakihama Y, Salamov AA, Savidor A, Scheuring CF, Smith BM, Sobral BW, Terry A, Torto-Alalibo TA, Win J, Xu Z, Zhang H, Grigoriev IV, Rokhsar DS, Boore JL. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006;313(5791):1261-6.
Usman HM, Tan Q, Karim MM, Adnan M, Yin W-X, Zhu F-X, Luo C-X. Sensitivity of Colletotrichum fructicola and Colletotrichum siamense of Peach in China to Multiple Classes of Fungicides and Characterization of Pyraclostrobin-Resistant Isolates. Plant Disease 2021;105(11):3459-3465.
Wang Y, Jin X, Rui H, Liu T, Hou J. Cold Temperature Regulation of Zoospore Release in Phytophthora sojae: The Genes That Differentially Expressed by Cold Temperature. Russian Journal of Genetics 2018;54(6):618-628.
Wu S, Guo Y, Adil MF, Sehar S, Cai B, Xiang Z, Tu Y, Zhao D, Shamsi IH. Comparative Proteomic Analysis by iTRAQ Reveals that Plastid Pigment Metabolism Contributes to Leaf Color Changes in Tobacco (Nicotiana tabacum) during Curing. Int J Mol Sci 2020;21(7):2394-2394.
Yasin N, Khan W, Ahmad S, Ahmad A, Akram W, Ijaz M. Role of Acinetobacter sp. CS9 in Improving Growth
and Phytoremediation Potential of Catharanthus
longifolius under Cadmium Stress. Polish Journal of Environmental Studies 2018a;28(1):435-443.
Yasin NA, Khan WU, Ahmad SR, Ali A, Ahmed S, Ahmad A. Effect of Bacillus fortis 162 on growth, oxidative stress tolerance and phytoremediation potential of Catharanthus roseus under chromium stress. International Journal of Agriculture and Biology 2018b;20(7):1513-1522.
Yousaf A, Qadir A, Anjum T, Ahmad A. Identification of Microbial Metabolites Elevating Vitamin Contents in Barley Seeds. Journal of Agricultural and Food Chemistry 2015;63(32):7304-10.
Zaheer MM, Yasin NA, Ahmad SR, Khan WU, Ahmad A, Ali A, Rehman SU. Amelioration of cadmium stress in gladiolus (Gladiolus grandiflora L.) by application of potassium and silicon. Journal of Plant Nutrition 2017;41(4):461-476.
Zhang H, Chang Z, Mehmood K, Yang M, Liu Z, Duan Z, Yuan F, Ali MM, Adnan M, Qasim M, Shaheen S, Abbas RZ, Tian Y, Guo R. Tetramethylpyrazine inhibited hypoxia-induced expression of calcium-sensing receptors in pulmonary artery smooth muscle cells in chickens. Journal of biological regulators and homeostatic agents 2018;32 3:489-495.
