Influence of crude oil pollution on the content and electrophoretic spectrum of proteins in Carex hirta plants at the initial stages of vegetative development

  • L. V. Bunіo Ivan Franko National University
  • O. M. Tsvilynyuk Ivan Franko National University
Keywords: adaptation syndrome; heat shock protein; abscisic acis (ABA); crude oil; soil.

Abstract

The role of proteins in the general adaptive response of Carex hirta plants to soil pollution by crude oil has been studied. It was established that a possible element of the process of adaptation of C. hirta plants to combined stress – conditions of soil polluted by crude oil – may be the synthesis of stress proteins – high molecular weight of more than 60 kD and low molecular weight, not exceeding 22–45 kD. The synthesis of all 5 HSP families was detected in the leaves and rhizomes, and only sHSP (starting from Mr 32 kD), Hsp 60 and Hsp 100 proteins were synthesized in the roots under the influence of crude oil pollution. The development of C. hirta adaptation syndrome under the influence of crude oil pollution of the soil was promoted by enhanced synthesis of proteins with Mr 85, 77, 64, 60 and 27 kD in the leaves, 118 and 41 kD in the rhizomes and proteins with Mr 105, 53, 50 and 43 kD in the roots of the plants. The decrease in the amount of proteins with Mr 91, 45, 28 kD in the leaves, proteins with Mr 85, 76 and 23 kD in rhizomes and proteins with Mr 64 and 39 in the roots of C. hirta plants under conditions of crude oil polluted soil could be a consequence of inhibition of synthesis or degradation of protein molecules providing the required level of low molecular weight protective compounds in cells. The root system and rhizomes of C. hirta plants undergo a greater crude oil load, which leads to increased protein synthesis in these organs and decreased in the leaves, correspondingly. However, a decrease in protein content in the leaves may indicate their outflow in the roots and rhizomes. Сrude oil contaminated soil as a polycomponent stressor accelerated the aging of leaves of C. hirta plants, which could be caused by increased synthesis of ABA. ABA in its turn induced the synthesis of leaf-specific protein with Mr 27 kD. These proteins bind significant amounts of water with their hydrate shells maintaining the high water holding capacity of the cytoplasm under drought conditions. ABA inhibits the mRNA synthesis and their corresponding proteins, which are characteristic under normal conditions, and induces the expression of genes and, consequently, the synthesis of specific proteins including 27 kD protein. By stimulating the expression of individual genes and the synthesis of new polypeptides, ABA promotes the formation of protective reactions and increases the resistance of plants to crude oil pollution.

References

Ali, A., Pardo, J. M., & Yun, D.-J., (2020). Desensitization of ABA-signaling: The swing from activation to degradation. Frontiers in Plant Science, 11, 379.

Al-Whaibi, M. H. (2011). Plant heat-shock proteins: A mini review. Journal of King Saud University – Science, 23, 139–150.

Alyammahi, O., & Gururani, M. A. (2020). Chlorophyll-a fluorescence analysis reveals differential response of photosynthetic machinery in melatonin-treated oat plants exposed to osmotic stress. Agronomy, 10(10), 15–20.

Banarjee, P. (2018). Phytoremediation: Using natural strength for curing nature. Acta Scientific Agriculture, 2(12), 144–153.

Bhakti, P., Negri, A. S., Failla, O., Scienza, A., & Espen, L. (2018). Root proteomic and metabolic analyses reveal specific responses to drought stress in differently tolerant grapevine rootstocks. BMC Plant Biology, 18, 126–152.

Bhat, R. A., Dervash, M. A., Mehmood, M. A., Rashid, A., Bhat, J. I. A., & Singh, D. V. (2017). Mycorrhizae: A sustainable industry for plant and soil environment. In: Mycorrhiza - nutrient uptake, biocontrol, ecorestoration. Издательство, город. Pp. 473–502.

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

Brady, C. A., & Attardi, L. D. (2010). p53 at a glance. Journal Cell Sci, 123, 2527–2532.

Bunio, L. V., & Tsvilynjuk, O. M. (2015). Specific features of morphogenesis of sedge (Carex hirta L.) on oil-contaminated soil. Contemporary Problems of Ecology, 8, 660–667.

Bunio, L., Vojtenko, L., Musatenko, L., Tsvilynjuk, О., & Terek, О. (2014b). Hormonalnyi status roslyn Carex hirta L., vyroshchenykh na hruntakh zabrudnenykh naftoiu [Hormonal status of Carex hirta L. plants grown on oil polluted soil]. Visnyk of Lviv University, Series Biology, 67, 274–282 (in Ukrainian).

Bunіo, L. V., Tsvilinjuk, O. M., & Terek, O. I. (2017). Zmina morfohenezu pidzemnykh orhaniv roslyn Sarex hirta L. za umov rostu na naftozabrudnenynomu grunti [Changes of morphogenesis undersoil organs of Carex hirta L. plants growing on the oilcontaminated soil]. Studia Biologica, 11 (3-4), 51–52 (in Ukrainian).

Carvalho, A., Nabais, C., Roiloa, S. R., & Rodriguez-Echeverria, S. (2013). Revegetation of abandoned copper mines: The role of seed banks and soil amendments. Web Ecology, 13, 69–77.

Chen, X., Lin, S., Liu, Q., Huang, J., Zhang, W., Lin, J., Wang, Y., Ke, Y., & He, H. (2014). Expression and interaction of small heat shock proteins (sHsps) in rice in response to heat stress. Biochim Biophys Acta, 1844, 818–828.

Chizhevskaya, M. V., Mironova, V. A., & Fomina, N. V. (2014). Rezultaty primenenija smeshannykh kultur pochvennykh vodoroslej dlya bioremediatsii pochv, zagriaznennykh nefteproduktami [The results of application of mixed cultures of soil algae for bioremediation of soils polluted by oil products]. Vestnik KrasGAU, Ecology, 12, 94–98 (in Russian).

Danylyk, I., & Kricsfalusy, V. V. (2020). Phytogeographical differentiation of the genus Carex (Cyperaceae) in Saskatchewan, Canada. Journal of Botany, 30(1), 1–21.

Danylyk, I., & Sosnovska, S. (2016). Strukturno-funktsionalni ta adaptatsijni peretvorennia v populiatsijakh vydiv rodu Carex L. u karpatskomu, podilskomu ta zakhidnopoliskomu rehionakh Ukrajiny v umovakh antropopresiji [Structural and functional changes and adaptive potential of Carex L. populations in the Ukrainian Carpathians and in the Western Polissia and Podillia regions (Ukraine) under anthropogenic pressure]. Naukovi Osnovy Zberezhennia Biotychnoi Riznomanitnosti, 7(14), 157–180 (in Ukrainian).

Danylyk, I., & Sosnovska, S. (2017). Population structure of Carex dioica L. (Cyperaceae) in Ukraine under different growth conditions. Biodiversity: Research and Conservation, 46, 19–33.

Dhanwal, P., Kumar, A., Dudeja, S., Chhokar, V., & Beniwal, V. (2017). Recent advances in phytoremediation technology. Advances in Environmental Biotechnology, ?????, 227–241.

Dickinson, N. (2017). Phytoremediation. Encyclopedia of Applied Plant Science, 3, 327–331.

Drozdova, Р., Bedulina, D., Madyarova, Е., Rivarola-Duarte, L., Schreiber, S., Stadler, Р. F., Luckenbach, T., & Timofeyev, M. (2019). Description of strongly heat-inducible heat shock protein 70 transcripts from Baikal endemic amphipods. Scientific Reports, 9, 8907.

Dwyer, S., Chow, W., Yamori, W., Evans, J., Kaines, S., Badger, M., & Caemmerer, S. (2012). Antisense reductions in the PsbO protein of photosystem II leads to decreased quantum yield but similar maximal photosynthetic rates. Journal Experimental Botani, 63(13), 4781–4795.

Dzhura, N. (2011). Perspektyvy fitoremediatsiji naftozabrudnenykh gruntiv roslynamy Faba bona Medic. (Vicia faba L.) [Prospects of oil polluted soils phytoremediation by Faba bona Medic. (Vicia faba L.) plants]. Visnyk of the Lviv University, Series Biology, 57, 117–124 (in Ukrainian).

Elekes, C. C. (2014). Eco-technological solutions for the remediation of polluted soil and heavy metal recovery. In: Hernández-Soriano, M. C. (Ed.). Environmental risk assessment of soil contamination. InTech, Rijeka. Pp. 309–335.

Emad, J., Kovalchuk, A., Raffaello, T., Keriö, S., Teeri, T., & Asiegbu, F. O. (2018). A gene encoding scots pine antimicrobial protein Sp-AMP2 (PR-19) confers increased tolerance against Botrytis cinerea in transgenic tobacco. Forests, 9(1), 10.

Fernandes, H., Michalska, K., Sikorski, M., & Jaskolski, M. (2013). Structural and functional aspects of PR-10 proteins. FEBS Journal, 280(5), 1169–1199.

Glibovytska, N., & Mykhailiuk, Y. (2020). Phytoindication research in the system of environmental monitoring. Ecological Sciences, 28, 111–114 (in Ukrainian).

González-Elizondo, M. S., Reznicek, A. A., & Tena-Flores, J. A. (2018). Cyperaceae in Mexico: Diversity and distribution. Botanical Sciences, 96(2), 305–331.

Gorshkova, О. G., Gudzenko, Т. V., Voliuvach, О. V., Beliaeva, Т. О., & Konup, І. Р. (2017). Oil oxidization and bio-safactants production by strains of P. fluorescens ONU541 and B. megaterium ONU542. Microbiology and Biotechnology, 2, 61–71 (in Ukrainian).

Gow-Jen, S., Lee-Feng, C., & Rong-Long, P. (2011). The extrinsic proteins of an oxygen-evolving complex in marine diatom Cylindrotheca fusiformis. Botanical Studies, 52, 161–171.

Gururani, M. A., Venkatesh, J., Ghosh, R., Strasser, R. J., Ponpandian, L. N., & Bae, H. (2017). Chlorophyll-a fluorescence evaluation of PEG-induced osmotic stress on PSII activity in Arabidopsis plants expressing SIP1. Plant Biosyst. International Journal Dealing with all Aspects of Plant Biology, 3504, 1–8.

Hamzah, A., & Priyadarshini, R. (2014). Identification of wild grass as remediator plant on artisanal gold mine tailing. Plant Science International, 1, 33–40.

Hasanuzzaman, M., Nahar, K., Alam, M., Roychowdhury, R., & Fujita, M. (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International Journal Molecular Sciences, 14(5), 9643–9684.

Ite, A. E., & Ibok, U. J. (2019). Role of plants and microbes in bioremediation of petroleum hydrocarbons contaminated soils. International Journal of Environmental Bioremediation and Biodegradation, 7(1), 1–19.

Jaber, E., Sooriyaarachchi, S., Covarrubias, S., Ubhayasekera, A. W., Mowbray, S. L., & Asiegbu, F. O. (2013). Molecular characterization of the expression and regulation of Scots pine (Pinus sylvestris L.) antimicrobial proteins (AMPs). In: XIII Conference root and butt rot of forest trees. Firenze University Press, Firenze. Pp. 26–28.

Jiménez-Mejías, P., Rodríguez-Palacios, G. E., Amini-Rad, М., & Martín-Bravo, S. (2015). Taxonomic notes on some problematic Carex (Cyperaceae) names from SW Asia. Phytotaxa, 219(2), 183–189.

Kamba, P. F., Dickson, D. A., White, N. A., Ekstrom, J. L., Koslowsky, D. J., & Hoogstraten, C. G. (2018). The 27 kDa Trypanosoma brucei pentatricopeptide repeat protein is a g-tract specific RNA binding protein. Scientific Reports, 8(1), 16989.

Katz, A., & Orellana, O. (2012). Protein synthesis and the stress response. In: Biyani, M. (Ed.). Cell-free protein synthesis. Издательство, город. Pp. 111–134.

 

465

Koopman, J., Aleksanyan, T., Aleksanyan, A., Fayvush, G., Oganesian, M., Vitek, E., & Więcław, H. (2021a). The genus Carex (Cyperaceae) in Armenia. Phytotaxa, 494, 1–41.

 

Koopman, J., Więcław, H., & Waltje, H. (2021b). Carex × terschellingensis hybr. nov. [= Carex acuta × C. trinervis] and Carex × reichgeltii hybr. nov. [= Carex acuta × C. aquatilis], Cyperaceae, found in the Netherlands. Gorteria – Dutch Botanical Archives, 43, 27–34.

Kosmala, A., Bocian, A., Rapacz, M., Jurczyk, B., & Zwierzykowski, Z. (2009). Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. Journal Experimental Botani, 60, 3595–3609.

Kosová, K., Vítámvás, P., Urban, M. O., Prášil, I. T., & Renaut, J. (2018). Plant abiotic stress proteomics: The major factors determining alterations in cellular proteome. Frontiers in Plant Science, 9, 122.

Kozeko, L. Y., Artemenko, O. A., Zaslavsky, V. A., Didukh, A. Y., Rahmetov, D. B., Martynyuk, G. M., Didukh, Y. P., & Kordyum, Y. L. (2011). Evaluation of plant state under unfavorable change of environmental conditions using heat shock protein 70 kDa (HSP 70). Ukrainian Botanical Journal, 68(6), 890–900 (in Ukrainian).

Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259), 680–684.

Laghlimi, R. M., Baghdad, B., Hadi, H., & Bouabdli, A. (2015). Phytoremediation mechanisms of heavy metal contaminated soils. Journal of Ecology, 5, 375–388.

Lario, L. D., Parra, E. R., & Gutierrez, C. (2013). Anti-silencing function proteins are involved in ultraviolet-induced DNA damage repair and are cell cycle regulated by E2F transcription factors in Arabidopsis. Plant Physiology, 162(2), 1164–1177.

Levine, A. J., & Oren, M. (2009). The first 30 years of p53: Growing ever more complex. Nature Reviews Cancer, 9(10), 749–758.

Li, N., Dejuan, E., Joon, Y. C., Zeng, L., Mengzhu, L., Li-Jun, H., & Yeon, K. W. (2021). Plant hormone-mediated regulation of heat tolerance in response to global climate change. Frontiers in Plant Science, 11, 627969.

Liu, H., & Charng, Y. (2012). Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signaling and Behavior, 7(5), 547–550.

Liu, H., Shi, J., Sun, C., Gong, H., Fan, X., Qiu, F., Huang, X., Feng, Q., Zheng, X., Yuan, N., Li, C., Zhang, Z., Deng, Y., Wang, J., Pan, G., Han, B., Lai, J., & Wu, Y. (2016). Gene duplication confers enhanced expression of 27-kDa γ-zein for endosperm modification in quality protein maize. Proc Natl Acad Sci USA, 113(18), 4964–4969.

Ma, H., Song, T., Wang, T., & Wang, S. (2016). Influence of human p53 on plant development. PLoS One, 11(9), 0162840.

Malik, N. A., Kumar, J., Wani, M. S., Tantray, Y. R., & Ahmad, T. (2021). Role of Mushrooms in the bioremediation of soil. Microbiota and Biofertilizers, 2, 77–102.

Mishra, D., Shekhar, S., Singh, D., Chakraborty, S., & Chakraborty, N. (2018). Heat shock proteins and abiotic stress tolerance in plants. In: Asea, A., & Kaur, P. (Eds.). Regulation of heat shock protein responses. Springer. Pp. 41–69.

Murzin, I. R., Kositsyna, A. A., Rozentsvet, O. A., & Makurina, O. N. (2011). Vliyanie ksenobiotikov na soderzhanie membrannosvyazannyih belkov v tkanyah vodnogo pogruzh Egeria densa [Xenobiotic effect on content of membrane proteins in tissue of water submerged plant Egeria densa]. Izvestiya Samarskogo Nauchnogo Tsentra RAN, 13(1), 257–259 (in Russian).

Nedjimi, B. (2021). Phytoremediation: A sustainable environmental technology for heavy metals decontamination. SN Applied Sciences, 3, 286.

Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., & Tran, L. S. (2014). ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytologist, 202, 35–49.

Pakharkova, N. V., Prudnikova, S. V., Gekk, A. S., Larkova, A. N., & Korosteleva, N. S. (2015). Optimizatsija vybora rastenij dlia bioremediatsiji pochv, zagryaznennykh neftiju i nefteproduktami v uslovijah Yuzhnoy Sibiri [Optimization of plant choice for bioremediation of soils contaminated with oil and oil products in the South Siberia conditions]. Vestnik KrasGAU, Biological Sciences, 8, 28–33 (in Russian).

Peco, J. D., Higueras, P., Campos, J. A., Esbrí, J. M., Moreno, M. M., Battaglia-Brunet, F., & Sandalio, L. M. (2021). Abandoned mine lands reclamation by plant remediation technologies. Sustainability, 13, 6555.

Pereira-Silva, L., Trevisan, R., Rodrigues, A. C., & Larridon, I. (2020). Combining the small South American genus Androtrichum into Cyperus (Cyperaceae). Plant Ecology and Evolution, 153(3), 446–454.

Qu, A. L., Ding, Y. F., Jiang, Q., & Zhu, C. (2013). Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun, 432, 203–207.

Romaniuk, O. I., Shevchyk, L. Z., & Zhak, T. V. (2018). The change of oil quantity and dynamics of soil phytotoxicity at the oil pollution. Scientific and Technical Journal, 18, 7–14 (in Ukrainian).

Roose, J. L., Frankel, L. K., Mummadisetti, M. P., & Bricker, T. M. (2016). The extrinsic proteins of photosystem II: Update. Planta, 243, 889–908.

Sasi, S., Venkatesh, J., Daneshi, R. F., & Gururani, M. A. (2018). Photosystem II extrinsic proteins and their putative role in abiotic stress tolerance in higher plants. Plants, 7, 100.

Shevchyk, L. Z., & Romanyuk, O. I. (2017). Analiz biolohichnykh sposobiv vidnovlennia naftozabrudnenykh gruntiv [Analysis of biological methods of recovery of oil-contaminated soils]. ScienceRise: Biological Science, 1(4), 31–39 (in Ukrainian).

Sliwiak, J., Sikorski, M., & Jaskolski, M. (2018). PR-10 proteins as potential mediators of melatonin-cytokinin cross talk in plants: Crystallographic studies of LlPR-10.2B isoform from yellow lupine. FEBS Journal, 285(10), 1907–1922.

Smith, P., House, J. I., & Mercedes, B. (2016). Global change pressures on soils from land use and management. Global Change Biol., 22(3), 1008–1028.

Stoychev, V., Simova-Stoilova, L., Vaseva, I., Kostadinova, A., Nenkova, R., Feller, U., & Demirevska, K. (2013). Protein changes and proteolytic degradation in red and white clover plants subjected to waterlogging. Acta Physiologiae Plantarum, 35(6), 1925–1932.

Taguchi, S., Shen, L., Han, G., Umena, Y., Shen, J.-R., Noguchi, T., & Mino, H. (2020). Formation of the high-spin S2 state related to the extrinsic proteins in the oxygen evolving complex of photosystem II. Journal of Physical Chemistry Letters, 11(20), 8908–8913.

Takahashi, F., Kuromori, T., Urano, K., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2020). Drought stress responses and resistance in plants: From cellular responses to long-distance intercellular communication. Frontiers in Plant Science, 11, 556972.

Tang, K. H. D. (2019). Phytoremediation of soil contaminated with petroleum hydrocarbons: A review of recent literature. Global Journal of Civil and Environmental Engineering, 1, 33–42.

Tian, F., Hu, X.-L., Yao, T., Yang, X., Chen, J.-G., Lu, M.-Z., & Zhang, J. (2021). Recent advances in the roles of HSFs and HSPs in heat stress response in woody plants. Frontiers in Plant Science, 12, 4905.

Tsvilinjuk, O., Bunіo, L., Karpyn, O., & Pentsak, A. (2017). Fitoremediatsija naftozabrudnenykh hruntiv za dopomohoju roslyn Carex hirta L. [Phytoremediation of oil contaminated soils using plants Carex hirta L.]. Construction, Material Science, Mechanical Engineering, 99, 187–193 (in Ukrainian).

Ul Haq, S., Khan, A., Ali, M., Khattak, A. M., Gai, W.-X., Zhang, H.-X., Wei, A.-M., & Gong, Z.-H. (2019). Heat shock proteins: Dynamic biomolecules to counter plant biotic and abiotic stresses. International Journal of Molecular Sciences, 20(21), 5321.

Villaverde, T., Jiménez-Mejías, P., Luceño, M., Waterway, M. J., Kim, S., Lee, B., Rincón-Barrado, M., Hahn, M., Maguilla, E., & Roalson, E. H. (2020). A new classification of Carex (Cyperaceae) subgenera supported by a HybSeq backbone phylogenetic tree. Botanical Journal of the Linnean Society, 194, 141–163.

Waters, E. R., & Vierling, E. (2020). Plant small heat shock proteins – evolutionary and functional diversity. New Phytologist, 227, 24–37.

Wawrzyńska, A., & Agnieszka, S. (2020). Proteasomal degradation of proteins is important for the proper transcriptional response to sulfur deficiency conditions in plants. Plant and Cell Physiology, 61(9), 1548–1564.

Zahermand, S., Vafaeian, M., & Bazyar, M. H. (2020). Analysis of the physical and chemical properties of soil contaminated with oil (petroleum) hydrocarbons. Earth Sciences Research Journal, 24(2), 163–168.

Zhang, L., Wang, Y., Zhang, Q., Jiang, Y., Zhang, H., & Li, R. (2020). Overexpression of HbMBF1a, encoding multiprotein bridging factor 1 from the halophyte Hordeum brevisubulatum, confers salinity tolerance and ABA insensitivity to transgenic Arabidopsis thaliana. Plant Molecular Biology, 102, 1–17.

Zhao, J., Lu, Z., Wang, L., & Jin, B. (2021). Plant responses to heat stress: Physiology, transcription, noncoding RNAs, and epigenetics. Journal of Molecular Sciences, 22, 117.

Published
2021-07-18
How to Cite
BunіoL. V., & Tsvilynyuk, O. M. (2021). Influence of crude oil pollution on the content and electrophoretic spectrum of proteins in Carex hirta plants at the initial stages of vegetative development . Regulatory Mechanisms in Biosystems, 12(3), 459-466. https://doi.org/10.15421/022163