Genomic exploration of HAK/KUP/KT potassium transporter genes in Citrus sinensis (L.) Osbeck: A comprehensive bioinformatics approach

Year 2024, Volume: 13 Issue: 3, 186 - 200, 31.12.2024

Ummahan Öz

https://doi.org/10.54187/jnrs.1553782

Abstract

Citrus sinensis (L.) Osbeck, a member of the Rutaceae family, holds significant economic importance. Potassium (K), an essential macronutrient, is vital in diverse physiological processes, such as photosynthesis, osmoregulation, stress tolerance, and disease resistance. The high-affinity K ion transporters (HAK), K ion uptake permeases (KUP), and K transporters (KT) gene family represents the largest group of K transporters. This study aims to comprehensively analyze HAK/KUP/KT genes in C. sinensis (Cs). Phylogenetic analysis, chromosome distribution, gene structure and conserved protein motif analysis, protein interaction, homology modeling, cis-acting element analysis, functional gene ontology, miRNA analysis, and primer search were performed using CsHAK sequences. Through bioinformatics tools, 25 CsHAK genes were identified and categorized into three distinct groups based on the results of phylogenetic analysis. Furthermore, it has been determined that CsHAK genes play a role in K transport, localizing in organelles and plasma membranes. They are found on the first, second, fifth, seventh, and eighth chromosomes. Furthermore, cis-acting elements associated with stress response and miRNAs have been identified. This study provides a robust foundation for future functional genomics research, offering insights into the genetic landscape of K transporters in C. sinensis. The findings contribute valuable information for crop improvement strategies and enhance our understanding of plant responses to environmental challenges.

Keywords

Bioinformatics, Cis-acting element, Citrus sinensis, miRNA, Potassium

Ethical Statement

No approval from the Board of Ethics is required.

References

• R. Johson, K. Vishwakarma, M. S. Hossen, V. Kumar, A. M. Shackira, J. T. Puthur, G. Abdi, M. Sarraf, M. Hasanuzzaman, Potassium in plants: Growth regulation, signaling, and environmental stress tolerance, Plant Physiology and Biochemistry 172 (2022) 56–69.
• X. Wang, P. Wu, X. Hu, S. Chang, M. Zhang, K. Zhang, S. Zhai, X. Yang, L. He, X. Guo, Identification and stress function verification of the HAK/KUP/KT family in Gossypium hirsutum, Gene 818 (2022) 1-10.
• F. Azeem, R. Zameer, M. A. Rehman Rashid, I. Rasul, S. Ul-Allah, M. H. Siddique, S. Fiaz, A. Raza, A. Younas, A. Rasool, M. A. Ali, S. Anwar, M. H. Siddiqui, Genome-wide analysis of potassium transport genes in Gossypium raimondii suggest a role of GrHAK/KUP/KT8, GrAKT2.1 and GrAKT1.1 in response to abiotic stress, Plant Physiology and Biochemistry 170 (2022) 110–122.
• R. Jin, W. Jiang, M. Yan, A. Zhang, M. Liu, P. Zhao, X. Chen, Z. Tang, Genome-wide characterization and expression analysis of HAK K+ transport family in Ipomoea, 3 Biotech 11 (1) (2021) 1–18.
• W. Li, G. Xu, A. Alli, L. Yu, Plant HAK/KUP/KT K+ transporters: Function and regulation, Seminars in Cell and Developmental Biology 74 (2018) 133–141.
• T. Yang, X. Lu, Y. Wang, Y. Xie, J. Ma, X. Cheng, E. Xia, X. Wan, Z. Zhang, HAK/KUP/KT family potassium transporter genes are involved in potassium deficiency and stress responses in tea plants (Camellia sinensis L.): Expression and functional analysis, BMC Genomics 21 (1) (2020) 1–18.
• E. O. Nestrerenko, O. E. Krasnoperova, S. V. Isayenkov, Potassium Transport Systems and Their Role in Stress Response, Plant Growth, and Development, Cytology and Genetics 55 (1) (2021) 63–79.
• S. Liu, B. Wu, Y. Xie, S. Zheng, J. Xie, W. Wang, D. Xiang, C. Li, Genome-wide analysis of HAK/KUP/KT potassium transporter genes in banana (Musa acuminata L.) and their tissue-specific expression profiles under potassium stress, Plant Growth Regulation 97 (1) (2022) 51–60.
• Y. Li, L. Peng, C. Xie, X. Shi, C. Dong, Q. Shen, Y. Xu, Genome-wide identification, characterization, and expression analyses of the HAK/KUP/KT potassium transporter gene family reveals their involvement in K+ deficient and abiotic stress responses in pear rootstock seedlings, Plant Growth Regulation 85 (2) (2018) 187–198.
• Q. Wan, T. Bai, M. Liu, Y. Liu, Y. Xie, T. Zhang, M. Huang, J. Zhang, Comparative Analysis of the Chalcone-Flavanone Isomerase Genes in Six Citrus Species and Their Expression Analysis in Sweet Orange (Citrus sinensis), Frontiers in Genetics 13 (April) (2022) 1-13.
• B. Acoglu, P. Y. Omeroglu, Effectiveness of different types of washing agents on reduction of pesticide residues in orange (Citrus sinensis), LWT- Food Science and Technology 147 (February) (2021) 1-12.
• Q. Xu, L. L. Chen, X. Ruan, D. Chen, A. Zhu, C. Chen, D. Bertrand, W. B. Jiao, B. H. Hao, M. P. Lyon, J. Chen, S. Gao, F. Xing, H. Lan, J. W. Chang, X. Ge, Y. Lei, Q. Hu, Y. Miao, L. Wang, S. Xiao, M. Kumar Biswas, W. Zeng, H. Cao, X. Yang, X. W. Xu, Y. J. Cheng, J. Xu, J. H. Liu, O. Junhong Luo, Z. Tang, W. W. Guo, H. Kuang, M. L. Roose, N. Nagarajan, X. X. Deng, Y. Ruan, The draft genome of sweet orange (Citrus sinensis), Nature Genetics 45 (1) (2013) 59–66.
• J. M. J. Favela-Hernández, O. González-Santiago, M. A. Ramírez-Cabrera, P. C. Esquivel-Ferriño, M. D. R. Camacho-Corona, Chemistry and pharmacology of Citrus sinensis, Molecules 21 (2) (2016) 247 1-24.
• C. Mannucci, F. Calapai, L. Cardia, G. Inferrera, G. D'Arena, M. Di Pietro, M. Navarra, S. Gangemi, E. Ventura Spagnolo, G. Calapai, Clinical pharmacology of Citrus aurantium and Citrus sinensis for the treatment of anxiety, Evidence-based Complementary and Alternative Medicine 2018 (2018) Article ID 3624094 18 pages.
• S. Kumar, S. Kumar, T. Mohapatra, Interaction Between Macro‐ and Micro-Nutrients in Plants, Frontiers in Plant Science 12 (May) (2021) Article Number 665583 9 pages.
• K. Işinkaralar, R. Erdem, The effect of atmospheric deposition on potassium accumulation in several tree species as a biomonitor, Environmental Research and Technology 5 (1) (2022) 94–100.
• N. T. Barlas, Citrus response to various foliar potassium treatments, Journal of Plant Nutrition 46 (9) (2023) 1920–1932.
• E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M. R. Wilkins, R. D. Appel, A. Bairoch, Protein Identification and Analysis Tools on the ExPASy Server, in: J.M. Walker, (Eds.), The Proteomics Protocols Handbook, Springer Protocols Handbooks, Humana Press, 2005, pp. 571–608.
• K. Tamura, G. Stecher, S. Kumar, MEGA11: Molecular Evolutionary Genetics Analysis Version 11, Molecular Biology and Evolution 38 (7) (2021) 3022–3027.
• I., Letunic, P. Bork, Interactive tree of life (iTOL) v5: An online tool for phylogenetic tree display and annotation, Nucleic Acids Research 49 (W1) (2021) W293–W296.
• J. Chao, Z. Li, Y. Sun, O. O. Aluko, X. Wu, Q. Wang, G. Liu, MG2C: a user-friendly online tool for drawing genetic maps, Molecular Horticulture 1 (1) (2021) 1–4.
• B. Hu, J. Jin, A. Y. Guo, H. Zhang, J. Luo, G. Gao, GSDS 2.0: An upgraded gene feature visualization server, Bioinformatics 31 (8) (2015) 1296–1297.
• T. L. Bailey, J. Johnson, C. E. Grant, W. S. Noble, The MEME Suite, Nucleic Acids Research 43 (W1) (2015) W39–W49.
• L. A. Kelley, S. Mezulis, C. M. Yates, M. N. Wass, M. J. Sternberg, The Phyre2 web portal for protein modeling, prediction and analysis, Nature Protocols 10 (6) (2016) 845–858.
• D. Szklarczyk, A. L. Gable, D. Lyon, A. Junge, S. Wyder, J. Huerta-Cepas, M. Simonovic, N. T., Morris, J. H. Doncheva, P. Bork, L. J. Jensen, C. Von Mering, STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets, Nucleic Acids Research 47 (D1) (2019) D607–D613.
• M. Lescot, P. Déhais, G. Thijs, K. Marchal, Y. Moreau, Y. Van De Peer, P. Rouzé, S. Rombauts, PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences, Nucleic Acids Research 30 (1) (2002) 325–327.
• X. Dai, P. X. Zhao, psRNATarget: A plant small RNA target analysis server, Nucleic Acids Research 39 (SUPPL. 2) (2011) 155–159.
• A. Kozomara, M. Birgaoanu, S. Griffiths-Jones, MiRBase: From microRNA sequences to function, Nucleic Acids Research 47 (D1) (2019) D155–D162.
• R. Kalendar, B. Khassenov, Y. Ramankulov, O. Samuilova, K. I. Ivanov, FastPCR: An in silico tool for fast primer and probe design and advanced sequence analysis, Genomics 109 (3–4) (2017) 312–319.
• R. Kalendar, D. Lee, A. H. Schulman, Java web tools for PCR, in silico PCR, and oligonucleotide assembly and analysis, Genomics, 98 (2) (2011) 137–144.
• Y. Gao, C. Yu, K. Zhang, H. Zhang, S. Zhang, Z. Song, Identification and characterization of the strawberry KT/HAK/KUP transporter gene family in response to K+ deficiency, Acta Physiologiae Plantarum 43 (1) (2021) 1–13.
• A. Khan, Z. Shah, S. Ali, N. Ahmad, M. Iqbal, A. Ullah, F. Ayub, Genome wide identification, structural characterization and phylogenetic analysis of High-Affinity potassium (HAK) ion transporters in common bean (Phaseolus vulgaris L.), BMC Genomic Data 24 (1) (2023) 1–13.
• X. Feng, Y. Wang, N. Zhang, Z. Wu, Q. Zeng, J. Wu, X. Wu, L. Wang, J. Zhang, Y. Qi, Genome-wide systematic characterization of the HAK/KUP/KT gene family and its expression profile during plant growth and in response to low-K+ stress in Saccharum, BMC Plant Biology, 20 (1) (2020) 1–17.
• K. Cai, F. Zeng, J. Wang, G. Zhang, Identification and characterization of HAK/KUP/KT potassium transporter gene family in barley and their expression under abiotic stress, BMC Genomics 22 (1) (2021) 1–14.
• Q. Li, W. Du, X. Tian, W. Jiang, B. Zhang, Y. Wang, Y. Pang, Genome-wide characterization and expression analysis of the HAK gene family in response to abiotic stresses in Medicago, BMC Genomics 23 (1) (2020) 1–19.
• M. M. Tahir, L. Tong, L. Xie, T. Wu, M. I. Ghani, X. Zhang, S. Li, X. Gao, L. Tariq, D. Zhang, Y. Shao, Identification of the HAK gene family reveals their critical response to potassium regulation during adventitious root formation in apple rootstock, Horticultural Plant Journal 9 (1) (2023) 45–59.
• J. Zhou, H. J. Zhou, P. Chen, L. L. Zhang, J. T. Zhu, P. F. Li, J. Yang, Y. Z. Ke, Y. H. Zhou, J. N. Li, H. Du, Genome-wide survey and expression analysis of the kt/hak/kup family in brassica napus and its potential roles in the response to k+ deficiency, International Journal of Molecular Sciences 21 (24) (2020) 1–19.
• Y. Wang, Y. Zhang, Y. Wei, J. Meng, C. Zhong, C. Fan, Characterization of HAK protein family in Casuarina equisetifolia and the positive regulatory role of CeqHAK6 and CeqHAK11 genes in response to salt tolerance, Frontiers in Plant Science, 13 (February) (2023) Article Number 1084337.
• A. Shafique, R. Batool, M. Rizwan, R. Zameer, H. Arshad, H. Xu, K. Alwutayd, H. AbdElgawad, F. Azeem, Integrative omics analysis of Rosa chinensis reveals insights into its transcriptome and in silico characterization of potassium transport genes, Plant Stress, 10 (July) (2023) Article Number 100202.
• Y., Chen, Y. Lin, S. Zhang, Z. Lin, S. Chen, Z. Wang, Genome-Wide Identification and Characterization of the HAK Gene Family in Quinoa (Chenopodium quinoa Willd.) and Their Expression Profiles under Saline and Alkaline Conditions, Plants, 12 (21) (2023) 1-14.
• F. Azeem, U. Ijaz, M. A. Ali, S. Hussain, M. Zubair, H. Manzoor, M. Abid, R. Zameer, D. S. Kim, K. S. Golokhvast, G. Chung, S. Sun, M. A. Nawaz, Genome-wide identification and expression profiling of potassium transport-related genes in Vigna radiata under abiotic stresses, Plants 11 (1) 2022 1-22.
• P. Guleria, M. Mahajan, J. Bhardwaj, S. K. Yadav, Plant Small RNAs: Biogenesis, Mode of Action and Their Roles in Abiotic Stresses, Genomics, Proteomics and Bioinformatics 9 (6) (2011) 183–199.
• L. I. Shukla, V. Chinnusamy, R. Sunkar, The role of microRNAs and other endogenous small RNAs in plant stress responses, Biochimica et Biophysica Acta - Gene Regulatory Mechanisms 1779 (11) (2008) 743–748.
• R. Sunkar, V. Chinnusamy, J. Zhu, J. K. Zhu, Small RNAs as big players in plant abiotic stress responses and nutrient deprivation, Trends in Plant Science 12 (7) (2007) 301–309.
• R. Tiwari, M. V. Rajam, RNA- and miRNA-interference to enhance abiotic stress tolerance in plants, Journal of Plant Biochemistry and Biotechnology 31 (4) (2022) 689–704.
• F. Zhang, J. Yang, N. Zhang, J. Wu, H. Si, Roles of microRNAs in abiotic stress response and characteristics regulation of plant, Frontiers in Plant Science 13 (2022) Article Number 919243 14 pages.