TY  - JOUR
T1  - Deciphering late embryogenesis abundant (LEA) genes in Phaseolus Vulgaris L. through bioinformatics
AU  - Büyük, İlker
AU  - Farhoomand Aksoy, Darya
AU  - Akbulut, Simay Ezgi
PY  - 2024
DA  - December
Y2  - 2024
DO  - 10.53447/communc.1440742
JF  - Communications Faculty of Sciences University of Ankara Series C  Biology
JO  - Commun. Fac. Sci. Univ. Ank. Ser. C
PB  - Ankara University
WT  - DergiPark
SN  - 1303-6025
SP  - 81
EP  - 108
VL  - 33
IS  - 2
LA  - en
AB  - The Late Embryogenesis Abundant (LEA) gene family is considered vital for plant's ability to survive freezing and desiccation, affecting important developmental and growth processes. These proteins possess notable hydrophilicity and thermal stability, which are essential for preserving cell membrane integrity, forming molecular barriers, aiding in ionic binding, and mitigating oxidative damage during extended periods of exposure to abiotic stress conditions. Although LEA proteins have been extensively studied in numerous plant species, this study represents the initial comprehensive exploration and characterization of LEA proteins in Phaseolus vulgaris L. In this context, the biochemical/physicochemical properties of the LEA family at both the gene and protein level have been deeply characterized and defined using various bioinformatics tools. Through comprehensive bioinformatics analyzes, we identified 80 LEA genes in common bean and phylogenetically categorized their proteins into eight major groups. Investigating gene duplications, we uncovered 28 events, including 24 segmental and 4 tandem duplications, significantly influencing the evolutionary trajectory of this gene family. In silico micro-RNA (miRNA) target analyzes revealed that 21 PvLEA genes were targeted by various miRNAs, with miRN2588 and miR164 being the most prevalent. PvLEA-63 emerged as the most highly expressed gene across tissues, followed by PvLEA-27, PvLEA-35, PvLEA-41, PvLEA-49 and PvLEA-52 genes, demonstrating their ubiquitous expression patterns. Moreover, using publicly available RNAseq data, a comparative expression study of PvLEA genes was carried out, and expression alterations in PvLEA-02, -08, -20, -21, -40, -42, -50 and -51 genes were detected under both salt and drought stress conditions. These results constitute a substantial resource for future researchers interested in unravelling the functional intricacies of PvLEA genes.
KW  - LEA gene family
KW  - Phaseolus vulgaris L.
KW  - bioinformatics
KW  - RNAseq
CR  - Rodríguez, L., Mendez, D., Montecino, H., Carrasco, B., Arevalo, B., Palomo, I., Fuentes, E., Role of Phaseolus vulgaris L. in the prevention of cardiovascular diseases—cardioprotective potential of bioactive compounds, Plants, 11 (2) (2022), 186. https://doi.org/10.3390/plants11020186
CR  - Nadeem, M. A., Yeken, M. Z., Shahid, M. Q., Habyarimana, E., Yılmaz, H., Alsaleh, A., Hatipoğlu, R., Çilesiz, Y., Khawar, K. M., Ludidi, N., Common bean as a potential crop for future food security: an overview of past, current and future contributions in genomics, transcriptomics, transgenics and proteomics, Biotechnology & Biotechnological Equipment, 35 (1) (2021), 759-787. https://doi.org/10.1080/13102818.2021.1920462
CR  - Yeken, M. Z., Özer, G., Çiftçi, V., Genome-wide identification and expression analysis of DGK (Diacylglycerol Kinase) genes in common bean, Journal of Plant Growth Regulation, 42 (4) (2023), 2558-2569. https://doi.org/10.1007/s00344-022-10726-x
CR  - Hutchins, A. M., Winham, D. M., Thompson, S. V., Phaseolus beans: impact on glycaemic response and chronic disease risk in human subjects, British Journal of Nutrition, 108 (S1) (2012), S52-S65. https://doi.org/10.1017/S0007114512000761
CR  - Büyük, İ., Okay, A., Gorska, M., Ilhan, E., Aras, E. S., Identification and characterization of the Pvul-GASA gene family in the Phaseolus vulgaris and expression patterns under salt stress, Turkish Journal of Botany, 45 (7) (2021), 655-670. https://doi.org/10.3906/bot-2101-13
CR  - Büyük, İ., Aras, S., Screening of PvLEA3 gene mRNA expression levels with qRT-PCR in different bean varieties (Phaseolus vulgaris L.) subjected to salt and drought stress, Turkish Journal of Botany, 39 (6) (2015), 1014-1020. https://doi.org/10.3906/bot-1502-4
CR  - Chen, Y., Li, C., Zhang, B., Yi, J., Yang, Y., Kong, C., Lei, C., Gong, M., The role of the late embryogenesis-abundant (LEA) protein family in development and the abiotic stress response: a comprehensive expression analysis of potato (Solanum tuberosum), Genes, 10 (2) (2019), 148. https://doi.org/10.3390/genes10020148
CR  - Geng, W., Wang, Y., Zhang, J., Liu, Z., Chen, X., Qin, L., Yang, L., Tang, H., Genome-wide identification and expression analyses of late embryogenesis abundant (LEA) gene family in tobacco (Nicotiana tabacum L.) reveal their function in abiotic stress responses, Gene, 836 (2022), 146665. https://doi.org/10.1016/j.gene.2022.146665
CR  - Hiz, M. C., Canher, B., Niron, H., Turet, M., Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions, PloS One, 9 (3) (2014), e92598. https://doi.org/10.1371/journal.pone.0092598
CR  - Yamaguchi-Shinozaki, K., Shinozaki, K., Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses, Annual Review of Plant Biology, 57 (2006), 781-803.  https://doi.org/10.1146/annurev.arplant.57.032905.105444
CR  - Gao, J., Lan, T., Functional characterization of the late embryogenesis abundant (LEA) protein gene family from Pinus tabuliformis (Pinaceae) in Escherichia coli, Scientific Reports, 6 (1) (2016), 19467. https://doi.org/10.1038/srep19467
CR  - Jin, X., Cao, D., Wang, Z., Ma, L., Tian, K., Liu, Y., Gong, Z., Zhu, X., Jiang, C., Li, Y., Genome-wide identification and expression analyses of the LEA protein gene family in tea plant reveal their involvement in seed development and abiotic stress responses, Scientific Reports, 9 (1) (2019), 14123.  https://doi.org/10.1038/s41598-019-50645-8
CR  - Magwanga, R. O., Lu, P., Kirungu, J. N., Lu, H., Wang, X., Cai, X., Zhou, Z., Zhang, Z., Salih, H., Wang, K., Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton, BMC Genetics, 19 (1) (2018), 1-31.  https://doi.org/10.1186/s12863-017-0596-1
CR  - Chen, J., Li, N., Wang, X., Meng, X., Cui, X., Chen, Z., Ren, H., Ma, J., Liu, H., Late embryogenesis abundant (LEA) gene family in Salvia miltiorrhiza: identification, expression analysis, and response to drought stress, Plant Signaling & Behavior, 16 (5) (2021), 1891769. 	https://doi.org/10.1080/15592324.2021.1891769
CR  - Ma, J., Zuo, D., Ye, H., Yan, Y., Li, M., Zhao, P., Genome-wide identification, characterization, and expression pattern of the late embryogenesis abundant (LEA) gene family in Juglans regia and its wild relatives J. mandshurica, BMC Plant Biology, 23 (1) (2023), 80. https://doi.org/10.1186/s12870-023-04096-z.
CR  - Leprince, O., Buitink, J., Desiccation tolerance: from genomics to the field, Plant Science, 179 (6) (2010), 554-564. https://doi.org/10.1016/j.plantsci.2010.02.011
CR  - Dure III, L., Greenway, S. C., Galau, G. A., Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis, Biochemistry, 20 (14) (1981), 4162-4168. https://doi.org/10.1021/bi00517a033
CR  - Hong-Bo, S., Zong-Suo, L., Ming-An, S., LEA proteins in higher plants: structure, function, gene expression and regulation, Colloids and Surfaces B: Biointerfaces, 45 (3-4) (2005), 131-135. https://doi.org/10.1016/j.colsurfb.2005.07.017
CR  - Hundertmark, M., Hincha, D. K., LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana, BMC Genomics, 9 (2008), 1-22. https://doi.org/10.1186/1471-2164-9-118
CR  - Liang, Y., Xiong, Z., Zheng, J., Xu, D., Zhu, Z., Xiang, J., Gan, J., Raboanatahiry, N., Yin, Y., Li, M., Genome-wide identification, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus, Scientific Reports, 6 (1) (2016), 24265. https://doi.org/10.1038/srep24265
CR  - Huang, R., Xiao, D., Wang, X., Zhan, J., Wang, A., He, L., Genome-wide identification, evolutionary and expression analyses of LEA gene family in peanut (Arachis hypogaea L.), BMC Plant Biology, 22 (1) (2022), 155. https://doi.org/10.1186/s12870-022-03462-7
CR  - Akbulut, S. E., Okay, A., Aksoy, T., Aras, E. S., Büyük, İ., The genome-wide characterization of WOX gene family in Phaseolus vulgaris L. during salt stress, Physiology and Molecular Biology of Plants, 28 (6) (2022), 1297-1309. https://doi.org/10.1007/s12298-022-01208-1
CR  - Wang, W., Gao, T., Chen, J., Yang, J., Huang, H., Yu, Y., The late embryogenesis abundant gene family in tea plant (Camellia sinensis): Genome-wide characterization and expression analysis in response to cold and dehydration stress, Plant Physiology and Biochemistry, 135 (2019), 277-286.  https://doi.org/10.1016/j.plaphy.2018.12.009
CR  - Chen, L., Xin, J., Song, H., Xu, F., Yang, H., Sun, H., Yang, M., Genome-wide study and functional characterization elucidates the potential association of late embryogenesis abundant (LEA) genes with lotus seed development, International Journal of Biological Macromolecules, 226 (2023), 1-13. https://doi.org/10.1016/j.ijbiomac.2022.11.301.
CR  - Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths‐Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., The Pfam protein families database, Nucleic Acids Research, 32 (1) (2004), D138-D141. https://doi.org/10.1093/nar/gkh121
CR  - Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., Phytozome: a comparative platform for green plant genomics, Nucleic Acids Research, 40 (D1) (2012), D1178-D1186. https://doi.org/10.1093/nar/gkr944
CR  - Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S. e., Wilkins, M. R., Appel, R. D., Bairoch, A. Protein Identification and Analysis Tools on the ExPASy Server. In: Walker, J.M. Editor. The Proteomics Protocols Handbook. Springer, (2005), 571-607. https://doi.org/10.1385/1-59259-890-0:571
CR  - Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C., Nakai, K., WoLF PSORT: protein localization predictor, Nucleic Acids Research, 35 (2) (2007), W585-W587. https://doi.org/10.1093/nar/gkm259
CR  - Thompson, J. D., Higgins, D. G., Gibson, T. J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Research, 22 (22) (1994), 4673-4680. https://doi.org/10.1093/nar/22.22.4673
CR  - Katoh, K., Standley, D. M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Molecular Biology and Evolution, 30 (4) (2013), 772-780. https://doi.org/10.1093/molbev/mst010
CR  - Letunic, I., Bork, P., Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation, Nucleic Acids Research, 49 (W1) (2021), W293-W296. https://doi.org/10.1093/nar/gkab301
CR  - Chen, C., Chen, H., Zhang, Y., Thomas, H. R., Frank, M. H., He, Y.,  Xia, R., TBtools: an integrative toolkit developed for interactive analyses of big biological data, Molecular Plant, 13 (8) (2020), 1194-1202.  https://doi.org/10.1016/j.molp.2020.06.009
CR  - Bailey, T. L., Johnson, J., Grant, C. E., Noble, W. S., The MEME suite, Nucleic Acids Research, 43 (W1) (2015), W39-W49. https://doi.org/10.1093/nar/gkv416
CR  - Yang, Z., Nielsen, R, Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models, Molecular Biology and Evolution, 17 (1) (2000), 32-43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
CR  - Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P., Rombauts, S., 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. https://doi.org/10.1093/nar/30.1.325
CR  - Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., Bourne, P. E., The protein data bank, Nucleic Acids Research, 28 (1) (2000), 235-242. https://doi.org/10.1093/nar/28.1.235
CR  - Kelley, L. A., Sternberg, M. J., Protein structure prediction on the Web: a case study using the Phyre server, Nature Protocols, 4 (3) (2009), 363-371. https://doi.org/10.1038/nprot.2009.2
CR  - Guo, Z., Kuang, Z., Wang, Y., Zhao, Y., Tao, Y., Cheng, C., Yang, J., Lu, X., Hao, C., Wang, T., PmiREN: a comprehensive encyclopedia of plant miRNAs, Nucleic Acids Research, 48 (D1) (2020), D1114-D1121. 
https://doi.org/10.1093/nar/gkz894
CR  - Dai, X., & Zhao, P. X., psRNATarget: a plant small RNA target analysis server, Nucleic Acids Research, 39 (suppl_2) (2011), W155-W159.  https://doi.org/10.1093/nar/gkr319
CR  - Kohl, M., Wiese, S., Warscheid, B., Cytoscape: software for visualization and analysis of biological networks, Data Mining in Proteomics: From Standards to Applications, (2011), 291-303. https://doi.org/10.1007/978-1-60761-987-1_18
CR  - Büyük, İ., Inal, B., Ilhan, E., Tanriseven, M., Aras, S., Erayman, M., Genome-wide identification of salinity responsive HSP70 s in common bean, Molecular Biology Reports, 43 (2016), 1251-1266. https://doi.org/10.1007/s11033-016-4057-0
CR  - Jorge, J. G., Villalobos-López, M. A., Chavarría-Alvarado, K. L., Ríos-Meléndez, S., López-Meyer, M., Arroyo-Becerra, A., Genome-wide transcriptional changes triggered by water deficit on a drought-tolerant common bean cultivar, BMC Plant Biology, 20 (1) (2020), 1-20. https://doi.org/10.1186/s12870-020-02664-1
CR  - Li, X., Cao, J., Late embryogenesis abundant (LEA) gene family in maize: identification, evolution, and expression profiles, Plant Molecular Biology Reporter, 34 (2016), 15-28. https://doi.org/10.1007/s11105-015-0901-y
CR  - Wang, X.S., Zhu, H.B., Jin, G.L., Liu, H.L., Wu, W.R., Zhu, J., Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.), Plant Science, 172 (2) (2007), 414-420. https://doi.org/10.1016/j.plantsci.2006.10.004
CR  - Celik Altunoglu, Y., Baloglu, P., Yer, E. N., Pekol, S., Baloglu, M. C., Identification and expression analysis of LEA gene family members in cucumber genome, Plant Growth Regulation, 80 (2016), 225-241. https://doi.org/10.1007/s10725-016-0160-4
CR  - Liu, H., Xing, M., Yang, W., Mu, X., Wang, X., Lu, F., Wang, Y., Zhang, L., Genome-wide identification of and functional insights into the late embryogenesis abundant (LEA) gene family in bread wheat (Triticum aestivum), Scientific Reports, 9 (1) (2019), 13375. https://doi.org/10.1038/s41598-019-49759-w
CR  - Nagaraju, M., Kumar, S. A., Reddy, P. S., Kumar, A., Rao, D. M., Kavi Kishor, P., Genome-scale identification, classification, and tissue specific expression analysis of late embryogenesis abundant (LEA) genes under abiotic stress conditions in Sorghum bicolor L., PloS One, 14 (1) (2019), e0209980.  https://doi.org/10.1371/journal.pone.0209980
CR  - Zan, T., Li, L., Li, J., Zhang, L., Li, X., Genome-wide identification and characterization of late embryogenesis abundant protein-encoding gene family in wheat: evolution and expression profiles during development and stress, Gene, 736 (2020), 144422. https://doi.org/10.1016/j.gene.2020.144422
CR  - Cao, J., Li, X., Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum), Planta, 241 (2015), 757-772. https://doi.org/10.1007/s00425-014-2215-y
CR  - Artur, M. A. S., Zhao, T., Ligterink, W., Schranz, E., Hilhorst, H. W., Dissecting the genomic diversification of late embryogenesis abundant (LEA) protein gene families in plants, Genome Biology and Evolution, 11 (2) (2019), 459-471. https://doi.org/10.1093/gbe/evy248
CR  - Jiang, Y., Zhang, S., Xu, H., Tian, H., Zhang, M., Zhu, S., Wang, C., Hou, J., Chen, G., Tang, X., Identification of the BcLEA gene family and functional analysis of the BcLEA73 gene in Wucai (Brassica campestris L.), Genes, 14 (2) (2023), 415. https://doi.org/10.3390/genes14020415
CR  - Jia, J.S., Ge, N., Wang, Q.Y., Zhao, L.T., Chen, C., Chen, J.W., Genome-wide identification and characterization of members of the LEA gene family in Panax notoginseng and their transcriptional responses to dehydration of recalcitrant seeds, BMC Genomics, 24 (1) (2023), 126. https://doi.org/10.1186/s12864-023-09229-0.
CR  - Aybüke, O., Sümer, A., Büyük, İ., Detailed characterization of lectin genes in common bean using bioinformatic tools, Communications Faculty of Sciences University of Ankara Series C Biology, 31 (1) (2022), 1-25. https://doi.org/10.53447/communc.1056557
CR  - Jia, C., Guo, B., Wang, B., Li, X., Yang, T., Li, N., Wang, J., Yu, Q., The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress, BMC Plant Biology, 22 (1) (2022), 596. https://doi.org/10.1186/s12870-022-03953-7
CR  - Huang, Z., Zhong, X.J., He, J., Jin, S.H., Guo, H.D., Yu, X.F., Zhou, Y.J., Li, X., Ma, M.D., Chen, Q.B., Genome-wide identification, characterization, and stress-responsive expression profiling of genes encoding LEA (late embryogenesis abundant) proteins in Moso bamboo (Phyllostachys edulis), PloS One, 11 (11) (2016), e0165953. https://doi.org/10.1371/journal.pone.0165953
CR  - Olvera-Carrillo, Y., Luis Reyes, J., Covarrubias, A. A., Late embryogenesis abundant proteins: versatile players in the plant adaptation to water limiting environments, Plant Signaling & Behavior, 6 (4) (2011), 586-589. https://doi.org/10.4161/psb.6.4.15042
CR  - Schilling, S., Kennedy, A., Pan, S., Jermiin, L. S., Melzer, R., Genome‐wide analysis of MIKC‐type MADS‐box genes in wheat: pervasive duplications, functional conservation and putative neofunctionalization, New Phytologist, 225 (1) (2020), 511-529. https://doi.org/10.1111/nph.16122
CR  - Chen, X., Wang, P., Gu, M., Lin, X., Hou, B., Zheng, Y., Sun, Y., Jin, S., Ye, N., R2R3-MYB transcription factor family in tea plant (Camellia sinensis): Genome-wide characterization, phylogeny, chromosome location, structure and expression patterns. Genomics, 113 (3) (2021), 1565-1578. https://doi.org/10.1016/j.ygeno.2021.03.033
CR  - Mehan, M. R., Freimer, N. B., Ophoff, R. A., A genome-wide survey of segmental duplications that mediate common human genetic variation of chromosomal architecture, Human Genomics, 1 (5) (2004), 1-10. https://doi.org/10.1186/1479-7364-1-5-335
CR  - Cheng, Z., Zhang, X., Yao, W., Zhao, K., Liu, L., Fan, G., Zhou, B., Jiang, T.,  Genome-wide search and structural and functional analyses for late embryogenesis-abundant (LEA) gene family in poplar, BMC Plant Biology, 21 (1) (2021), 1-17. https://doi.org/10.1186/s12870-021-02872-3
CR  - Jiang, S.-Y., González, J. M., Ramachandran, S., Comparative genomic and transcriptomic analysis of tandemly and segmentally duplicated genes in rice, PloS One, 8  (5) (2013), e63551. https://doi.org/10.1371/journal.pone.0063551
CR  - Hurst, L. D., The Ka/Ks ratio: diagnosing the form of sequence evolution, Trends in Genetics, 18 (9) (2002), 486-487.  https://doi.org/10.1016/S0168-9525(02)02722-1
CR  - Koonin, E. V., Rogozin, I. B., Getting positive about selection, BioMed Central, (2003). https://doi.org/10.1186/gb-2003-4-8-331
CR  - Lohani, N., Golicz, A. A., Singh, M. B., Bhalla, P. L., Genome-wide analysis of the Hsf gene family in Brassica oleracea and a comparative analysis of the Hsf gene family in B. oleracea, B. rapa and B. napus, Functional & Integrative Genomics, 19 (2019), 515-531. https://doi.org/10.1007/s10142-018-0649-1
CR  - Lan, T., Gao, J., Zeng, Q.-Y., Genome-wide analysis of the LEA (late embryogenesis abundant) protein gene family in Populus trichocarpa, Tree Genetics & Genomes, 9 (2013), 253-264. 
https://doi.org/10.1007/s11295-012-0551-2
CR  - Yamaguchi-Shinozaki, K., Shinozaki, K., Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters, Trends in Plant Science, 10 (2) (2005), 88-94. https://doi.org/10.1016/j.tplants.2004.12.012
CR  - Niu, L., Chu, H. D., Tran, C. D., Nguyen, K. H., Pham, H. X., Le, D. T., Li, W., Wang, W., Le, T. D., Tran, L.-S. P., The GATA gene family in chickpea: structure analysis and transcriptional responses to abscisic acid and dehydration treatments revealed potential genes involved in drought adaptation, Journal of Plant Growth Regulation, 39 (2020), 1647-1660. https://doi.org/10.1007/s00344-020-10201-5
CR  - Shariatipour, N., Heidari, B., Meta-analysis of expression of the stress tolerance associated genes and uncover their-regulatory elements in rice (L.), The Open Bioinformatics Journal, 13 (1) (2020). https://doi.org/10.2174/1875036202013010039
CR  - Ain-Ali, Q.U., Mushtaq, N., Amir, R., Gul, A., Tahir, M., Munir, F., Genome-wide promoter analysis, homology modeling and protein interaction network of dehydration responsive element binding (DREB) gene family in Solanum tuberosum, PloS One, 16 (12) (2021), e0261215. https://doi.org/10.1371/journal.pone.0261215
CR  - Büyük, İ., Okay, A., Aras, S., Identification and characterization of SRS genes in Phaseolus vulgaris genome and their responses under salt stress, Biochemical Genetics, (2022), 1-22. https://doi.org/10.1007/s10528-021-10108-0
CR  - Singh, S., Cornilescu, C. C., Tyler, R. C., Cornilescu, G., Tonelli, M., Lee, M. S., Markley, J. L. Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress‐related protein, Protein Science, 14 (10) (2005), 2601-2609. https://doi.org/10.1110/ps.051579205
CR  - Akbulut, S. E., Şafak, Z., Okay, A., Amirina, K., Büyük, İ., EIN3/EIL (Ethylene insensitive3/Ethylene insensitive3 like) protein family in Phaseolus vulgaris: Identification, evolution and expression analysis within the genome, Turkish Journal of Agriculture-Food Science and Technology, 11 (2) (2023), 215-226. https://doi.org/10.24925/turjaf.v11i2.215-226.5172
CR  - Kavas, M., Abdulla, M. F., Mostafa, K., Seçgin, Z., Yerlikaya, B. A., Otur, Ç., Gökdemir, G., Kurt Kızıldoğan, A., Al-Khayri, J. M., Jain, S. M., Investigation and expression analysis of R2R3-MYBs and anthocyanin biosynthesis-related genes during seed color development of common bean (Phaseolus vulgaris), Plants, 11 (23) (2022), 3386. https://doi.org/10.3390/plants11233386
CR  - Guo, H.S., Xie, Q., Fei, J.F., & Chua, N.H., MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development, The Plant Cell, 17 (5) (2005), 1376-1386. https://doi.org/10.1105/tpc.105.030841
CR  - Kim, Y.S., Kim, S.G., Park, J.E., Park, H.Y., Lim, M.H., Chua, N.H., Park, C.M., A membrane-bound NAC transcription factor regulates cell division in Arabidopsis, The Plant Cell, 18 (11) (2006), 3132-3144. https://doi.org/10.1105/tpc.106.043018
CR  - Lu, S., Sun, Y. H., Chiang, V. L., Stress‐responsive microRNAs in Populus, The Plant Journal, 55 (1) (2008), 131-151. https://doi.org/10.1111/j.1365-313X.2008.03497.x
CR  - Wang, T., Chen, L., Zhao, M., Tian, Q., Zhang, W.H., Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing, BMC Genomics, 12 (1) (2011), 1-11. https://doi.org/10.1186/1471-2164-12-367
CR  - Chen, Y., Cao, J., Comparative genomic analysis of the Sm gene family in rice and maize, Gene, 539 (2) (2014), 238-249. https://doi.org/10.1016/j.gene.2014.02.006.
CR  - Khodajou-Masouleh, H., Shahangian, S. S., Attar, F., H. Sajedi, R., Rasti, B., Characteristics, dynamics and mechanisms of actions of some major stress-induced biomacromolecules; addressing Artemia as an excellent biological model, Journal of Biomolecular Structure and Dynamics, 39 (15) (2021), 5619-5637. https://doi.org/10.1080/07391102.2020.1796793
UR  - https://doi.org/10.53447/communc.1440742
L1  - https://dergipark.org.tr/en/download/article-file/3744370
ER  -