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Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors

Year 2024, Volume: 11 Issue: 3, 305 - 314, 09.12.2024
https://doi.org/10.19159/tutad.1531506

Abstract

This study investigated the regulation of gene expression in root, leaf, and grain tissues of bread wheat (Triticum aestivum L.) in response to drought and heat stresses at the grain-filling stage for the first time by transcriptome analysis. The sequencing result, obtained on a Roche 454 GS FLX+, yielded a total of 117,790,028 base reads and 8,351 unigenes with an average length of 461 bp. Through transcriptome analysis, numerous transcripts have been identified to be involved in maintaining osmotic and ionic balance, detecting and transmitting signals, modifying protein structure and function, ensuring membrane integrity and stability, and are associated with energy and carbohydrate metabolism. Against drought and high-temperature stresses, tolerance mechanisms in the root, leaf, and grain tissues differentially regulated many specific transcription factors identified. Betaine aldehyde dehydrogenase, callose synthase, cell wall-associated hydrolase, MYB33, and NAC69 transcription factors expression levels were measured with qRT-PCR. Transcriptome analysis revealed that the transcripts identified were related to osmotic and ionic balance, signal detection and transduction, modification of structural and functional proteins, cell membrane structure and stability, energy and carbohydrate metabolism, and their expression level varied according to the tissue or drought and high-temperature stress applied.

References

  • Adel, S., Carels, N., 2023. Plant tolerance to drought stress with emphasis on wheat. Plants, 12(11): 1-26.
  • Anonymous, 2015a. International Wheat Genome Sequencing Consortium. (http://plants.ensebl.org/ Triticumaestivum/Info/Index), (Accessed Date: 15.11.2015).
  • Anonymous, 2015b. Plant Transcription Factor Database. (http://planttfdb.cbi.edu.cn), (Accessed Date: 18.12.2015).
  • Anonymous, 2021. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA (Accessed Date: 12.05.2021).
  • Chaidee, A., Pfeiffer, W., 2006. Parameters for cellular viability and membrane function in chenopodium cells show a specific response of extracellular pH to heat shock with extreme Q10. Plant Biology, 8(1): 42-51.
  • Chinnusamy, V., Zhu, J.K., 2009. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology, 12(2): 133-139.
  • Chunhua, Y., Dayong, L, Xue, L., Chengjun, J., Lili, H., Xianfeng, Z., 2014. OsMYB103L, an R2R3-MYB transcription factor, influence leaf rolling and mechanical strength inrice (Oryza sativa L.). BMC Plant Biology, 14(158): 1-15. Fahad, S., Bajwa, A.A., Nazir. U., Anjum, S.A., Sadia, S., Nasim, W., 2017. Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science, 8: 265598.
  • Field, D., Tiwari, B., Booth, T., Houten, S., Swan, D., Bertrand, N., Thurston, M., 2006. Open software for biologists: From famine to feast. Nature Biotechnology, 24(7): 801-803.
  • Fischer, T., Byerlee, D., Edmeades, G., 2014. Crop Yields and Global Food Security. Australian Centre for International Agricultural Research, Union Offset, Australia.
  • Hawkins, R.D., Hon, G.C., Ren, B., 2010. Next-generation genomics: An integrative approach. Nature Reviews Genetics, 11(7): 476-486.
  • Lal, M.K., Tiwari, R.K., Gahlaut, V., Mangal, V., Kumar, A., Singh, M.P., 2021. Physiological and molecular insights on wheat responses to heat stress. Plant Cell Reports, 41(3): 501-518.
  • Lu, L.J., Zhang, W.Y., Sun, L.J., Zhao, A.J., Zhang, Y.J., Wang, L.M., 2020. Gene co-expression network analysis to identify critical modules and candidate genes of drought-resistance in wheat. PloS One, 15(8): e0236186.
  • Mikołajczak, K., Kuczyńska, A., Krajewski, P., Kempa, M., 2023. Transcriptome profiling disclosed the effect of single and combined drought and heat stress on reprogramming of genes expression in barley flag leaf. Front in Plant Science, 13: 1096685.
  • Miralles, D.J., Abeledo, L.G., Prado, S.A., Chenu, K., Serrago, R.A., Savin, R., 2021. Crop physiology case histories for major crops. In: V.O. Sadras and D.F. Calderini (Eds.), Wheat, 1st Eds., Elsevier, Amsterdam, pp. 164-195.
  • Mornkham, T., Wangsomnuk, P.P., Fu, Y.B., Wangsomnuk, P., Jogloy, S., Patanothai, A., 2013. Extractions of high quality RNA from the seeds of Jerusalem Artichoke and other plant species with high levels of starch and lipid. Plants, 2(2): 302-316.
  • Mursalova, J., Akparov, Z., Ojaghi, J., Eldarov, M., Belen, S., Gummadov, N., Morgounov, A., 2015. Evaluation of drought tolerance of winter bread wheat genotypes under drip irrigation and rain-fed conditions. Turkish Journal of Agriculture and Forestry, 39(5): 817-824.
  • Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K., 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta, 1819(2): 97-103.
  • Nakashima, K., Yamaguchi-Shinozaki, K., Shinozaki, K., 2014. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science, 5: 170.
  • Nouraei, S., Mia, M.S., Liu, H., Turner, N.C., Yan, G., 2022. Transcriptome analyses of near isogenic lines reveal putative drought tolerance controlling genes in wheat. Frontiers in Plant Science, 13: 857829.
  • Park, E.J., Jeknic, Z., Sakamoto, A., Denoma, J., Yuwansiri, R., Murata, N., Chen, T.H., 2004. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. The Plant Journal, 40(4): 474-487.
  • Pequeno, D.N., Hernandez-Ochoa, I.M., Reynolds, M., Sonder, K., MoleroMilan, A., Robertson, R.D., 2021. Climate impact and adaptation to heat and drought stress of regional and global wheat production. Environmental Research Letters, 16(5): 054070.
  • Pour-Aboughadareh, A., Mohammadi, R., Etminan, A., Shooshtari, L., Maleki-Tabrizi, N., Poczai, P., 2020. Effects of drought stress on some agronomic and morpho-physiological traits in durum wheat genotypes. Sustainability, 12(14): 5610.
  • Pradhan, G.P., Prasad, P.V., Fritz, A.K., Kirkham, M B., Gill., B.S., 2012. Effects of drought and high temperature stress on synthetic hexaploid wheat. Functional Plant Biology, 39(3): 190-198.
  • Qin, D., Wu, H., Peng, H., Yao, Y., Ni, Z., Li, Z., 2008. Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using wheat genome array. BMC Genomics, 9: 432.
  • Rahaie, M., Xue, G.P., Naghavi, M.R., Alizadeh, H., Schenk, P.M., 2010. A MYB gene from wheat (Triticum aestivum L.) is up-regulated during salt and drought stresses and differentially regulated between salt-tolerant and sensitive genotypes. Plant Cell Reports, 29(8): 835-844.
  • Rizhsky, L., Liang, H., Mittler, R., 2002. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology, 130(3): 1143-1151.
  • Rontein, D., Basset, G., Hanson, A.D., 2002. Metabolic engineering of osmo protectant accumulation in plants. Metabolic Engineering, 4(1): 49-56.
  • Sabagh, A.E.L., Hossain, A., Islam, M.S., Iqbal, M.A., Amanet, K., Mubeen, M., Nasim, W., Wasaya, A., Llanes, A., Ratnasekera, D., Singhal, R.K., Kumari, A., Meena, R.S., Abdelhamid, M., Hasanuzzaman, M., Raza, M.A., Özyazici, G., Ozyazici, M.A., Erman, M., 2021. Prospective role of plant growth regulators for tolerance to abiotic stresses. In: T. Aftab and K.R. Hakeem (Eds.), Plant Growth Regulators, 1st Eds., Springer, Cham., Switzerland, pp. 1-38.
  • Saidi, M.N., Mahjoubi, H., Yacoubi., I., 2023. Transcriptome meta-analysis of abiotic stresses-responsive genes and identification of candidate transcription factors for broad stress tolerance in wheat. Protoplasma, 260(3): 707-721.
  • Sareen, S., Budhlakoti, N., Mishra, K.K., Bharad, S., Potdukhe, N.R., Tyagi, B.S., Singh, G.P., 2023. Resilience to terminal drought, heat, and their combination stress in wheat genotypes. Agronomy, 13(3): 891.
  • Senapati, N., Stratonovitch, P., Paul, M.J., Semenov, M.A., 2019. Drought tolerance during reproductive development is important for increasing wheat yield potential under climate change in Europe. Journal of Experimental Botany, 70(9): 2549-2560.
  • Shiriga, K., Sharma, R., Kumar, K., Yadav, S.K., Hossain, F., Thirunavukkarasu, N., 2014. Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene, 2(1): 407-417.
  • Trachtenberg, E.A., Holcomb, C.L., 2013. Transplantation immunology: Methods and protocols. In: A. Zachary (Ed.), Next-Generation HLA Sequencing Using the 454 GS FLX System, 2rd Edn., Springer, USA, pp. 197-219.
  • Turktas, M., Inal, B., Okay, S., Erkilic, E.G., Dundar, E., Hernandez, P., Dorado, G., Unver, T., 2013. Nutrition metabolism plays an important role in the alternate bearing of the olive tree (Olea europaea L.). PloS One, 8(3): e59876.
  • Vranić, M., Perochon, A., Doohan, F.M., 2023. Transcriptional profiling reveals the wheat defences against fusarium head blight disease regulated by a NAC transcription factor. Plants, 12(14): 2708.
  • Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 18(1): 1-14.
  • Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. A role of plant heat-shock proteins and molecular chaperones in abiotic stress response. Trends in Plant Science, 9(5): 244-252.
  • Wang, G., Zhang, X., Li, F., Luo, Y., Wang, W., 2010. Over accumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica, 48(1): 117-126.
  • Xi, W. Hao, C., Li, T., Wang, H., Zhang, X., 2023. Transcriptome analysis of roots from wheat (Triticum aestivum L.) varieties in response to drought stress. International Journal of Molecular Sciences, 24(8): 7245.

Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors

Year 2024, Volume: 11 Issue: 3, 305 - 314, 09.12.2024
https://doi.org/10.19159/tutad.1531506

Abstract

This study investigated the regulation of gene expression in root, leaf, and grain tissues of bread wheat (Triticum aestivum L.) in response to drought and heat stresses at the grain-filling stage for the first time by transcriptome analysis. The sequencing result, obtained on a Roche 454 GS FLX+, yielded a total of 117,790,028 base reads and 8,351 unigenes with an average length of 461 bp. Through transcriptome analysis, numerous transcripts have been identified to be involved in maintaining osmotic and ionic balance, detecting and transmitting signals, modifying protein structure and function, ensuring membrane integrity and stability, and are associated with energy and carbohydrate metabolism. Against drought and high-temperature stresses, tolerance mechanisms in the root, leaf, and grain tissues differentially regulated many specific transcription factors identified. Betaine aldehyde dehydrogenase, callose synthase, cell wall-associated hydrolase, MYB33, and NAC69 transcription factors expression levels were measured with qRT-PCR. Transcriptome analysis revealed that the transcripts identified were related to osmotic and ionic balance, signal detection and transduction, modification of structural and functional proteins, cell membrane structure and stability, energy and carbohydrate metabolism, and their expression level varied according to the tissue or drought and high-temperature stress applied.

References

  • Adel, S., Carels, N., 2023. Plant tolerance to drought stress with emphasis on wheat. Plants, 12(11): 1-26.
  • Anonymous, 2015a. International Wheat Genome Sequencing Consortium. (http://plants.ensebl.org/ Triticumaestivum/Info/Index), (Accessed Date: 15.11.2015).
  • Anonymous, 2015b. Plant Transcription Factor Database. (http://planttfdb.cbi.edu.cn), (Accessed Date: 18.12.2015).
  • Anonymous, 2021. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA (Accessed Date: 12.05.2021).
  • Chaidee, A., Pfeiffer, W., 2006. Parameters for cellular viability and membrane function in chenopodium cells show a specific response of extracellular pH to heat shock with extreme Q10. Plant Biology, 8(1): 42-51.
  • Chinnusamy, V., Zhu, J.K., 2009. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology, 12(2): 133-139.
  • Chunhua, Y., Dayong, L, Xue, L., Chengjun, J., Lili, H., Xianfeng, Z., 2014. OsMYB103L, an R2R3-MYB transcription factor, influence leaf rolling and mechanical strength inrice (Oryza sativa L.). BMC Plant Biology, 14(158): 1-15. Fahad, S., Bajwa, A.A., Nazir. U., Anjum, S.A., Sadia, S., Nasim, W., 2017. Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science, 8: 265598.
  • Field, D., Tiwari, B., Booth, T., Houten, S., Swan, D., Bertrand, N., Thurston, M., 2006. Open software for biologists: From famine to feast. Nature Biotechnology, 24(7): 801-803.
  • Fischer, T., Byerlee, D., Edmeades, G., 2014. Crop Yields and Global Food Security. Australian Centre for International Agricultural Research, Union Offset, Australia.
  • Hawkins, R.D., Hon, G.C., Ren, B., 2010. Next-generation genomics: An integrative approach. Nature Reviews Genetics, 11(7): 476-486.
  • Lal, M.K., Tiwari, R.K., Gahlaut, V., Mangal, V., Kumar, A., Singh, M.P., 2021. Physiological and molecular insights on wheat responses to heat stress. Plant Cell Reports, 41(3): 501-518.
  • Lu, L.J., Zhang, W.Y., Sun, L.J., Zhao, A.J., Zhang, Y.J., Wang, L.M., 2020. Gene co-expression network analysis to identify critical modules and candidate genes of drought-resistance in wheat. PloS One, 15(8): e0236186.
  • Mikołajczak, K., Kuczyńska, A., Krajewski, P., Kempa, M., 2023. Transcriptome profiling disclosed the effect of single and combined drought and heat stress on reprogramming of genes expression in barley flag leaf. Front in Plant Science, 13: 1096685.
  • Miralles, D.J., Abeledo, L.G., Prado, S.A., Chenu, K., Serrago, R.A., Savin, R., 2021. Crop physiology case histories for major crops. In: V.O. Sadras and D.F. Calderini (Eds.), Wheat, 1st Eds., Elsevier, Amsterdam, pp. 164-195.
  • Mornkham, T., Wangsomnuk, P.P., Fu, Y.B., Wangsomnuk, P., Jogloy, S., Patanothai, A., 2013. Extractions of high quality RNA from the seeds of Jerusalem Artichoke and other plant species with high levels of starch and lipid. Plants, 2(2): 302-316.
  • Mursalova, J., Akparov, Z., Ojaghi, J., Eldarov, M., Belen, S., Gummadov, N., Morgounov, A., 2015. Evaluation of drought tolerance of winter bread wheat genotypes under drip irrigation and rain-fed conditions. Turkish Journal of Agriculture and Forestry, 39(5): 817-824.
  • Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K., 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta, 1819(2): 97-103.
  • Nakashima, K., Yamaguchi-Shinozaki, K., Shinozaki, K., 2014. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science, 5: 170.
  • Nouraei, S., Mia, M.S., Liu, H., Turner, N.C., Yan, G., 2022. Transcriptome analyses of near isogenic lines reveal putative drought tolerance controlling genes in wheat. Frontiers in Plant Science, 13: 857829.
  • Park, E.J., Jeknic, Z., Sakamoto, A., Denoma, J., Yuwansiri, R., Murata, N., Chen, T.H., 2004. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. The Plant Journal, 40(4): 474-487.
  • Pequeno, D.N., Hernandez-Ochoa, I.M., Reynolds, M., Sonder, K., MoleroMilan, A., Robertson, R.D., 2021. Climate impact and adaptation to heat and drought stress of regional and global wheat production. Environmental Research Letters, 16(5): 054070.
  • Pour-Aboughadareh, A., Mohammadi, R., Etminan, A., Shooshtari, L., Maleki-Tabrizi, N., Poczai, P., 2020. Effects of drought stress on some agronomic and morpho-physiological traits in durum wheat genotypes. Sustainability, 12(14): 5610.
  • Pradhan, G.P., Prasad, P.V., Fritz, A.K., Kirkham, M B., Gill., B.S., 2012. Effects of drought and high temperature stress on synthetic hexaploid wheat. Functional Plant Biology, 39(3): 190-198.
  • Qin, D., Wu, H., Peng, H., Yao, Y., Ni, Z., Li, Z., 2008. Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using wheat genome array. BMC Genomics, 9: 432.
  • Rahaie, M., Xue, G.P., Naghavi, M.R., Alizadeh, H., Schenk, P.M., 2010. A MYB gene from wheat (Triticum aestivum L.) is up-regulated during salt and drought stresses and differentially regulated between salt-tolerant and sensitive genotypes. Plant Cell Reports, 29(8): 835-844.
  • Rizhsky, L., Liang, H., Mittler, R., 2002. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology, 130(3): 1143-1151.
  • Rontein, D., Basset, G., Hanson, A.D., 2002. Metabolic engineering of osmo protectant accumulation in plants. Metabolic Engineering, 4(1): 49-56.
  • Sabagh, A.E.L., Hossain, A., Islam, M.S., Iqbal, M.A., Amanet, K., Mubeen, M., Nasim, W., Wasaya, A., Llanes, A., Ratnasekera, D., Singhal, R.K., Kumari, A., Meena, R.S., Abdelhamid, M., Hasanuzzaman, M., Raza, M.A., Özyazici, G., Ozyazici, M.A., Erman, M., 2021. Prospective role of plant growth regulators for tolerance to abiotic stresses. In: T. Aftab and K.R. Hakeem (Eds.), Plant Growth Regulators, 1st Eds., Springer, Cham., Switzerland, pp. 1-38.
  • Saidi, M.N., Mahjoubi, H., Yacoubi., I., 2023. Transcriptome meta-analysis of abiotic stresses-responsive genes and identification of candidate transcription factors for broad stress tolerance in wheat. Protoplasma, 260(3): 707-721.
  • Sareen, S., Budhlakoti, N., Mishra, K.K., Bharad, S., Potdukhe, N.R., Tyagi, B.S., Singh, G.P., 2023. Resilience to terminal drought, heat, and their combination stress in wheat genotypes. Agronomy, 13(3): 891.
  • Senapati, N., Stratonovitch, P., Paul, M.J., Semenov, M.A., 2019. Drought tolerance during reproductive development is important for increasing wheat yield potential under climate change in Europe. Journal of Experimental Botany, 70(9): 2549-2560.
  • Shiriga, K., Sharma, R., Kumar, K., Yadav, S.K., Hossain, F., Thirunavukkarasu, N., 2014. Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene, 2(1): 407-417.
  • Trachtenberg, E.A., Holcomb, C.L., 2013. Transplantation immunology: Methods and protocols. In: A. Zachary (Ed.), Next-Generation HLA Sequencing Using the 454 GS FLX System, 2rd Edn., Springer, USA, pp. 197-219.
  • Turktas, M., Inal, B., Okay, S., Erkilic, E.G., Dundar, E., Hernandez, P., Dorado, G., Unver, T., 2013. Nutrition metabolism plays an important role in the alternate bearing of the olive tree (Olea europaea L.). PloS One, 8(3): e59876.
  • Vranić, M., Perochon, A., Doohan, F.M., 2023. Transcriptional profiling reveals the wheat defences against fusarium head blight disease regulated by a NAC transcription factor. Plants, 12(14): 2708.
  • Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 18(1): 1-14.
  • Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. A role of plant heat-shock proteins and molecular chaperones in abiotic stress response. Trends in Plant Science, 9(5): 244-252.
  • Wang, G., Zhang, X., Li, F., Luo, Y., Wang, W., 2010. Over accumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica, 48(1): 117-126.
  • Xi, W. Hao, C., Li, T., Wang, H., Zhang, X., 2023. Transcriptome analysis of roots from wheat (Triticum aestivum L.) varieties in response to drought stress. International Journal of Molecular Sciences, 24(8): 7245.
There are 39 citations in total.

Details

Primary Language English
Subjects Plant Biotechnology in Agriculture
Journal Section Research Article
Authors

Ebru Derelli Tüfekçi 0000-0003-1097-8574

Güray Akdogan 0000-0002-1192-3615

Mine Türktaş 0000-0001-8089-3774

Serkan Uranbey 0000-0002-0312-8099

Publication Date December 9, 2024
Submission Date August 10, 2024
Acceptance Date November 7, 2024
Published in Issue Year 2024 Volume: 11 Issue: 3

Cite

APA Derelli Tüfekçi, E., Akdogan, G., Türktaş, M., Uranbey, S. (2024). Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors. Türkiye Tarımsal Araştırmalar Dergisi, 11(3), 305-314. https://doi.org/10.19159/tutad.1531506
AMA Derelli Tüfekçi E, Akdogan G, Türktaş M, Uranbey S. Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors. TÜTAD. December 2024;11(3):305-314. doi:10.19159/tutad.1531506
Chicago Derelli Tüfekçi, Ebru, Güray Akdogan, Mine Türktaş, and Serkan Uranbey. “Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum Aestivum L.) in Response to Combined Abiotic Stress Factors”. Türkiye Tarımsal Araştırmalar Dergisi 11, no. 3 (December 2024): 305-14. https://doi.org/10.19159/tutad.1531506.
EndNote Derelli Tüfekçi E, Akdogan G, Türktaş M, Uranbey S (December 1, 2024) Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors. Türkiye Tarımsal Araştırmalar Dergisi 11 3 305–314.
IEEE E. Derelli Tüfekçi, G. Akdogan, M. Türktaş, and S. Uranbey, “Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors”, TÜTAD, vol. 11, no. 3, pp. 305–314, 2024, doi: 10.19159/tutad.1531506.
ISNAD Derelli Tüfekçi, Ebru et al. “Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum Aestivum L.) in Response to Combined Abiotic Stress Factors”. Türkiye Tarımsal Araştırmalar Dergisi 11/3 (December 2024), 305-314. https://doi.org/10.19159/tutad.1531506.
JAMA Derelli Tüfekçi E, Akdogan G, Türktaş M, Uranbey S. Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors. TÜTAD. 2024;11:305–314.
MLA Derelli Tüfekçi, Ebru et al. “Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum Aestivum L.) in Response to Combined Abiotic Stress Factors”. Türkiye Tarımsal Araştırmalar Dergisi, vol. 11, no. 3, 2024, pp. 305-14, doi:10.19159/tutad.1531506.
Vancouver Derelli Tüfekçi E, Akdogan G, Türktaş M, Uranbey S. Organ-Specific Gene Expression Profiles of Bread Wheat (Triticum aestivum L.) in Response to Combined Abiotic Stress Factors. TÜTAD. 2024;11(3):305-14.

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