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Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome

Year 2019, Volume: 19 Issue: 3, 299 - 309, 23.12.2019
https://doi.org/10.17475/kastorman.662581

Abstract

Aim of study: LEA proteins have a critical role in the abiotic stress response of plants. Ash belongs to the olive family and its genome sequence is complete. The LEA genes has not been extensively analyzed, although there are annotations in the ash genome. Therefore, it was aimed to perform genome-wide analysis of LEA genes in ash genome using bioinformatic tools in this study.
Materials and methods: Ash and LEA protein sequences were obtained from the Ash Tree Genome and LEAP database respectively. Homologous LEA peptides in ash were found using CLC Genomic Workbench 11. Properties of ash LEA proteins were determined with Expasy PROTPARAM. MEGA7 was used to construct the phylogenetic tree. Functional analysis of ash LEA proteins was carried out via Blast2GO. miRNAs targeting transcripts of ash LEA proteins were detected with psRNATarget. The three-dimensional structures of ash LEA proteins were predicted using PHYRE2.
Main result: 118 LEA genes (FexLEA) were identified in ash genome. FexLEA were divided into 5 distinct clusters according to phylogenetic analysis. The major molecular function of FexLEA was found as the binding activity. miR838 was the most common miRNA targeting FexLEA transcripts.
Highlights: This study will provide the basis for further functional analysis of LEA proteins in ash.

References

  • Akdogan, G., Tufekci, E. D., Uranbey, S. & Unver, T. (2016). miRNA-based drought regulation in wheat. Functional & Integrative Genomics, 16(3), 221-233.
  • Alsheikh, M. K., Svensson, J. T. & Randall, S. K. (2005). Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant, Cell & Environment, 28(9), 1114-1122.
  • Altunoglu, Y. C., Baloglu, M. C., Baloglu, P., Yer, E. N. & Kara, S. (2017). Genome-wide identification and comparative expression analysis of LEA genes in watermelon and melon genomes. Physiology and Molecular Biology of Plants, 23(1), 5-21.
  • Altunoglu, Y. C., Baloglu, P., Yer, E. N., Pekol, S. & Baloglu, M. C. (2016). Identification and expression analysis of LEA gene family members in cucumber genome. Plant Growth Regulation, 80(2), 225-241.
  • Bailey, T. L. & Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proceedings of the 2nd International Conference on Intelligent Systems for Molecular Biology, 148, 28-36.
  • Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F. & Covarrubias, A. A. (2008). The enigmatic LEA proteins and other hydrophilins. PlantPphysiology, 148(1), 6-24.
  • Beck, E. H., Fettig, S., Knake, C., Hartig, K. & Bhattarai, T. (2007). Specific and unspecific responses of plants to cold and drought stress. Journal of Biosciences, 32(3), 501-510.
  • Bravo, L. A., Gallardo, J., Navarrete, A., Olave, N., Martínez, J., Alberdi, M., ... & Corcuera, L. J. (2003). Cryoprotective activity of a cold‐induced dehydrin purified from barley. Physiologia Plantarum, 118(2), 262-269.
  • Candar‐Cakir, B., Arican, E. & Zhang, B. (2016). Small RNA and degradome deep sequencing reveals drought‐and tissue‐specific micrornas and their important roles in drought‐sensitive and drought‐tolerant tomato genotypes. Plant Biotechnology Journal, 14(8), 1727-1746.
  • Cao, J. & Li, X. (2015). Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum). Planta, 241(3), 757-772.
  • Charfeddine, S., Saïdi, M. N., Charfeddine, M. & Gargouri-Bouzid, R. (2015). Genome-wide identification and expression profiling of the late embryogenesis abundant genes in potato with emphasis on dehydrins. Molecular Biology Reports, 42(7), 1163-1174.
  • Conesa, A. & Götz, S. (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008(2008,619832), 1-12.
  • Dai, X. & Zhao, P. X. (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 39(suppl_2), W155-W159.
  • Dure III, L., Greenway, S. C. & Galau, G. A. (1981). 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), 4162-4168.
  • Filiz, E., Ozyigit, I. I., Tombuloglu, H. & Koc, I. (2013). In silico comparative analysis of LEA (Late Embryogenesis Abundant) proteins in Brachypodium distachyon L. Plant Omics, 6(6), 433.
  • Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L. & Salazar, G. A. (2015). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research, 44(D1), D279-D285.
  • Gasteiger, E., Hoogland, C., Gattiker, A., Wilkins, M. R., Appel, R. D. & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook (pp. 571-607). Humana press.
  • Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J. & Rokhsar, D. S. (2011). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40(D1), D1178-D1186.
  • Goyal, K., Walton, L. J. & Tunnacliffe, A. (2005). LEA proteins prevent protein aggregation due to water stress. Biochemical Journal, 388(1), 151-157.
  • Grelet, J., Benamar, A., Teyssier, E., Avelange-Macherel, M. H., Grunwald, D. & Macherel, D. (2005). Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiology, 137(1), 157-167.
  • Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S. & Masmoudi, K. (2011). Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signaling & Behavior, 6(10), 1503-1509.
  • Hara, M., Terashima, S. & Kuboi, T. (2001). Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. Journal of Plant Physiology, 158(10), 1333-1339.
  • Honjoh, K. I., Matsumoto, H., Shimizu, H., Ooyama, K., Tanaka, K., Oda, Y., ... & Iio, M. (2000). Cryoprotective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Bioscience, Biotechnology, and Biochemistry, 64(8), 1656-1663.
  • Huang, Z., Zhong, X. J., He, J., Jin, S. H., Guo, H. D., Yu, X. F. & Long, H. (2016). 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), e0165953.
  • Hunault, G. & Jaspard, E. (2010). LEAPdb: a database for the late embryogenesis abundant proteins. Bmc Genomics, 11(1), 221.
  • Hundertmark, M. & Hincha, D. K. (2008). LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics, 9(1), 118.
  • Kozomara, A. & Griffiths-Jones, S. (2013). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research, 42(D1), D68-D73.
  • Krüger, C., Berkowitz, O., Stephan, U. W. & Hell, R. (2002). A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. Journal of Biological Chemistry, 277(28), 25062-25069.
  • Kumar, S., Stecher, G. & Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874.
  • Lan, T., Gao, J. & Zeng, Q. Y. (2013). Genome-wide analysis of the LEA (late embryogenesis abundant) protein gene family in Populus trichocarpa. Tree Genetics & Genomes, 9(1), 253-264.
  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H. & Thompson, J. D. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947-2948.
  • Li, X. & Cao, J. (2016). Late Embryogenesis Abundant (LEA) gene family in maize: identification, evolution, and expression profiles. Plant Molecular Biology Reporter, 34(1), 15-28.
  • Li, X., Hou, Y., Zhang, L., Zhang, W., Quan, C., Cui, Y. & Bian, S. (2014). Computational identification of conserved microRNAs and their targets from expression sequence tags of blueberry (Vaccinium corybosum). Plant Signaling & Behavior, 9(9), e29462.
  • Li, L., Xu, H., Yang, X., Li, Y. & Hu, Y. (2011). Genome-wide identification, classification and expression analysis of LEA gene family in soybean. Scientia Agricultura Sinica, 44(19), 3945-3954.
  • Liang, Y., Xiong, Z., Zheng, J., Xu, D., Zhu, Z., Xiang, J. & Li, M. (2016). Genome-wide identification, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus. Scientific Reports, 6, 24265.
  • Lynch, M. & Conery, J. S. (2000). The evolutionary fate and consequences of duplicate genes. Science, 290(5494), 1151-1155.
  • Najafabadi, A. S. & Naghavi, M. R. (2018). Mining Ferula gummosa transcriptome to identify miRNAs involved in the regulation and biosynthesis of terpenes. Gene, 645, 41-47.
  • Pedrosa, A. M., Martins, C. D. P. S., Gonçalves, L. P. & Costa, M. G. C. (2015). Late embryogenesis abundant (LEA) constitutes a large and diverse family of proteins involved in development and abiotic stress responses in sweet orange (Citrus sinensis L. Osb.). PLoS One, 10(12), e0145785.
  • Ramachandran, V., & Chen, X. (2008). Small RNA metabolism in Arabidopsis. Trends in Plant Science, 13(7), 368-374.
  • Reyes, J. L., Rodrigo, M. J., Colmenero-Flores, J. M., Gil, J. V., Garay-Arroyo, A., Campos, F., ... & Covarrubias, A. A. (2005). Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant, Cell & Environment, 28(6), 709-718.
  • Semizer-Cuming, D., Kjær, E. D. & Finkeldey, R. (2017). Gene flow of common ash (Fraxinus excelsior L.) in a fragmented landscape. PloS One, 12(10), e0186757.
  • Shao, F., Qiu, D. & Lu, S. (2015). Comparative analysis of the Dicer-like gene family reveals loss of miR162 target site in SmDCL1 from Salvia miltiorrhiza. Scientific Reports, 5, 9891.
  • Sharma, M. & Laxmi, A. (2016). Jasmonates: emerging players in controlling temperature stress tolerance. Frontiers in Plant Science, 6, 1129.
  • Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W. & Thompson, J. D. (2011). Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7(1), 539.
  • Singh, N., Srivastava, S. & Sharma, A. (2016). Identification and analysis of miRNAs and their targets in ginger using bioinformatics approach. Gene, 575(2), 570-576.
  • Singh, S., Cornilescu, C. C., Tyler, R. C., Cornilescu, G., Tonelli, M., Lee, M. S. & Markley, J. L. (2005). Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress‐related protein. Protein Science, 14(10), 2601-2609.
  • Sollars, E. S., Harper, A. L., Kelly, L. J., Sambles, C. M., Ramirez-Gonzalez, R. H., Swarbreck, D., ... & Worswick, G. (2017). Genome sequence and genetic diversity of European ash trees. Nature, 541(7636), 212.
  • Srivastava, S., Srivastava, A. K., Suprasanna, P. & D’souza, S. F. (2012). Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. Journal of Experimental Botany, 64(1), 303-315.
  • Suyama, M., Torrents, D. & Bork, P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34(suppl_2), W609-W612.
  • Tolleter, D., Jaquinod, M., Mangavel, C., Passirani, C., Saulnier, P., Manon, S. & Macherel, D. (2007). Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. The Plant Cell, 19(5), 1580-1589.
  • Tunnacliffe, A. & Wise, M. J. (2007). The continuing conundrum of the LEA proteins. Naturwissenschaften, 94(10), 791-812.
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LEA Genlerinin Dişbudak (Fraxinus excelsior) Genomunda Tanımlanması ve Karakterizasyonu

Year 2019, Volume: 19 Issue: 3, 299 - 309, 23.12.2019
https://doi.org/10.17475/kastorman.662581

Abstract

Çalışmanın amacı: LEA proteinleri, bitkilerin abiyotik stres koşullarına tepki vermesinde önemli rol oynamaktadır. Dişbudak zeytingiller ailesinden genom dizisi tamamlanmış bir ağaç türüdür. Dişbudak genomunda LEA genlerine dair açıklamalar bulunsa da kapsamlı bir analiz yoktur. Bu sebeple, bu çalışmada biyoinformatik araçlar kullanılarak LEA genlerinin dişbudak genomunda detaylı analizinin yapılması amaçlanmıştır.
Materyal ve yöntem: Ash ve LEA protein dizileri sırasıyla Ash Tree Genome ve LEAP veri tabanından elde edilmiştir. Homolog dişbudak LEA peptitleri, CLC Genomic Workbench 11 kullanılarak bulunmuştur. Dişbudak LEA proteinlerinin özellikleri, Expasy PROTPARAM ile belirlenmiştir. MEGA7 filogenetik ağaç oluşturmak için kullanılmıştır. Dişbudak LEA proteinlerinin fonksiyonel analizi, Blast2GO ile gerçekleştirilmiştir. Dişbudak LEA proteinlerinin transkriptlerini hedef alan miRNA'lar psRNATarget ile tespit edilmiştir. Dişbudak LEA proteinlerinin üç boyutlu yapıları, PHYRE2 kullanılarak tahmin edilmiştir.
Sonuçlar: Dişbudak genomunda 118 tane LEA geni (FexLEA) tanımlanmıştır. FexLEA’lar filogenetik analize göre 5 dala ayrılmıştır. Fex-LEA üyelerinin başlıca moleküler fonksiyonu bağlanma aktivitesidir. miR838'in FexLEA transkriptlerini hedef alan en yaygın miRNA olduğu görülmüştür.
Önemli vurgular: Bu çalışma, dişbudak LEA proteinlerinin fonksiyonel analizleri için temel sağlayacaktır.

References

  • Akdogan, G., Tufekci, E. D., Uranbey, S. & Unver, T. (2016). miRNA-based drought regulation in wheat. Functional & Integrative Genomics, 16(3), 221-233.
  • Alsheikh, M. K., Svensson, J. T. & Randall, S. K. (2005). Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant, Cell & Environment, 28(9), 1114-1122.
  • Altunoglu, Y. C., Baloglu, M. C., Baloglu, P., Yer, E. N. & Kara, S. (2017). Genome-wide identification and comparative expression analysis of LEA genes in watermelon and melon genomes. Physiology and Molecular Biology of Plants, 23(1), 5-21.
  • Altunoglu, Y. C., Baloglu, P., Yer, E. N., Pekol, S. & Baloglu, M. C. (2016). Identification and expression analysis of LEA gene family members in cucumber genome. Plant Growth Regulation, 80(2), 225-241.
  • Bailey, T. L. & Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proceedings of the 2nd International Conference on Intelligent Systems for Molecular Biology, 148, 28-36.
  • Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F. & Covarrubias, A. A. (2008). The enigmatic LEA proteins and other hydrophilins. PlantPphysiology, 148(1), 6-24.
  • Beck, E. H., Fettig, S., Knake, C., Hartig, K. & Bhattarai, T. (2007). Specific and unspecific responses of plants to cold and drought stress. Journal of Biosciences, 32(3), 501-510.
  • Bravo, L. A., Gallardo, J., Navarrete, A., Olave, N., Martínez, J., Alberdi, M., ... & Corcuera, L. J. (2003). Cryoprotective activity of a cold‐induced dehydrin purified from barley. Physiologia Plantarum, 118(2), 262-269.
  • Candar‐Cakir, B., Arican, E. & Zhang, B. (2016). Small RNA and degradome deep sequencing reveals drought‐and tissue‐specific micrornas and their important roles in drought‐sensitive and drought‐tolerant tomato genotypes. Plant Biotechnology Journal, 14(8), 1727-1746.
  • Cao, J. & Li, X. (2015). Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum). Planta, 241(3), 757-772.
  • Charfeddine, S., Saïdi, M. N., Charfeddine, M. & Gargouri-Bouzid, R. (2015). Genome-wide identification and expression profiling of the late embryogenesis abundant genes in potato with emphasis on dehydrins. Molecular Biology Reports, 42(7), 1163-1174.
  • Conesa, A. & Götz, S. (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008(2008,619832), 1-12.
  • Dai, X. & Zhao, P. X. (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 39(suppl_2), W155-W159.
  • Dure III, L., Greenway, S. C. & Galau, G. A. (1981). 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), 4162-4168.
  • Filiz, E., Ozyigit, I. I., Tombuloglu, H. & Koc, I. (2013). In silico comparative analysis of LEA (Late Embryogenesis Abundant) proteins in Brachypodium distachyon L. Plant Omics, 6(6), 433.
  • Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L. & Salazar, G. A. (2015). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research, 44(D1), D279-D285.
  • Gasteiger, E., Hoogland, C., Gattiker, A., Wilkins, M. R., Appel, R. D. & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook (pp. 571-607). Humana press.
  • Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J. & Rokhsar, D. S. (2011). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40(D1), D1178-D1186.
  • Goyal, K., Walton, L. J. & Tunnacliffe, A. (2005). LEA proteins prevent protein aggregation due to water stress. Biochemical Journal, 388(1), 151-157.
  • Grelet, J., Benamar, A., Teyssier, E., Avelange-Macherel, M. H., Grunwald, D. & Macherel, D. (2005). Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiology, 137(1), 157-167.
  • Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S. & Masmoudi, K. (2011). Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signaling & Behavior, 6(10), 1503-1509.
  • Hara, M., Terashima, S. & Kuboi, T. (2001). Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. Journal of Plant Physiology, 158(10), 1333-1339.
  • Honjoh, K. I., Matsumoto, H., Shimizu, H., Ooyama, K., Tanaka, K., Oda, Y., ... & Iio, M. (2000). Cryoprotective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Bioscience, Biotechnology, and Biochemistry, 64(8), 1656-1663.
  • Huang, Z., Zhong, X. J., He, J., Jin, S. H., Guo, H. D., Yu, X. F. & Long, H. (2016). 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), e0165953.
  • Hunault, G. & Jaspard, E. (2010). LEAPdb: a database for the late embryogenesis abundant proteins. Bmc Genomics, 11(1), 221.
  • Hundertmark, M. & Hincha, D. K. (2008). LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics, 9(1), 118.
  • Kozomara, A. & Griffiths-Jones, S. (2013). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research, 42(D1), D68-D73.
  • Krüger, C., Berkowitz, O., Stephan, U. W. & Hell, R. (2002). A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. Journal of Biological Chemistry, 277(28), 25062-25069.
  • Kumar, S., Stecher, G. & Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874.
  • Lan, T., Gao, J. & Zeng, Q. Y. (2013). Genome-wide analysis of the LEA (late embryogenesis abundant) protein gene family in Populus trichocarpa. Tree Genetics & Genomes, 9(1), 253-264.
  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H. & Thompson, J. D. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947-2948.
  • Li, X. & Cao, J. (2016). Late Embryogenesis Abundant (LEA) gene family in maize: identification, evolution, and expression profiles. Plant Molecular Biology Reporter, 34(1), 15-28.
  • Li, X., Hou, Y., Zhang, L., Zhang, W., Quan, C., Cui, Y. & Bian, S. (2014). Computational identification of conserved microRNAs and their targets from expression sequence tags of blueberry (Vaccinium corybosum). Plant Signaling & Behavior, 9(9), e29462.
  • Li, L., Xu, H., Yang, X., Li, Y. & Hu, Y. (2011). Genome-wide identification, classification and expression analysis of LEA gene family in soybean. Scientia Agricultura Sinica, 44(19), 3945-3954.
  • Liang, Y., Xiong, Z., Zheng, J., Xu, D., Zhu, Z., Xiang, J. & Li, M. (2016). Genome-wide identification, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus. Scientific Reports, 6, 24265.
  • Lynch, M. & Conery, J. S. (2000). The evolutionary fate and consequences of duplicate genes. Science, 290(5494), 1151-1155.
  • Najafabadi, A. S. & Naghavi, M. R. (2018). Mining Ferula gummosa transcriptome to identify miRNAs involved in the regulation and biosynthesis of terpenes. Gene, 645, 41-47.
  • Pedrosa, A. M., Martins, C. D. P. S., Gonçalves, L. P. & Costa, M. G. C. (2015). Late embryogenesis abundant (LEA) constitutes a large and diverse family of proteins involved in development and abiotic stress responses in sweet orange (Citrus sinensis L. Osb.). PLoS One, 10(12), e0145785.
  • Ramachandran, V., & Chen, X. (2008). Small RNA metabolism in Arabidopsis. Trends in Plant Science, 13(7), 368-374.
  • Reyes, J. L., Rodrigo, M. J., Colmenero-Flores, J. M., Gil, J. V., Garay-Arroyo, A., Campos, F., ... & Covarrubias, A. A. (2005). Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant, Cell & Environment, 28(6), 709-718.
  • Semizer-Cuming, D., Kjær, E. D. & Finkeldey, R. (2017). Gene flow of common ash (Fraxinus excelsior L.) in a fragmented landscape. PloS One, 12(10), e0186757.
  • Shao, F., Qiu, D. & Lu, S. (2015). Comparative analysis of the Dicer-like gene family reveals loss of miR162 target site in SmDCL1 from Salvia miltiorrhiza. Scientific Reports, 5, 9891.
  • Sharma, M. & Laxmi, A. (2016). Jasmonates: emerging players in controlling temperature stress tolerance. Frontiers in Plant Science, 6, 1129.
  • Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W. & Thompson, J. D. (2011). Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7(1), 539.
  • Singh, N., Srivastava, S. & Sharma, A. (2016). Identification and analysis of miRNAs and their targets in ginger using bioinformatics approach. Gene, 575(2), 570-576.
  • Singh, S., Cornilescu, C. C., Tyler, R. C., Cornilescu, G., Tonelli, M., Lee, M. S. & Markley, J. L. (2005). Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress‐related protein. Protein Science, 14(10), 2601-2609.
  • Sollars, E. S., Harper, A. L., Kelly, L. J., Sambles, C. M., Ramirez-Gonzalez, R. H., Swarbreck, D., ... & Worswick, G. (2017). Genome sequence and genetic diversity of European ash trees. Nature, 541(7636), 212.
  • Srivastava, S., Srivastava, A. K., Suprasanna, P. & D’souza, S. F. (2012). Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. Journal of Experimental Botany, 64(1), 303-315.
  • Suyama, M., Torrents, D. & Bork, P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34(suppl_2), W609-W612.
  • Tolleter, D., Jaquinod, M., Mangavel, C., Passirani, C., Saulnier, P., Manon, S. & Macherel, D. (2007). Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. The Plant Cell, 19(5), 1580-1589.
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There are 56 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Aslı Uğurlu Bayarslan 0000-0003-2131-2823

Publication Date December 23, 2019
Published in Issue Year 2019 Volume: 19 Issue: 3

Cite

APA Uğurlu Bayarslan, A. (2019). Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome. Kastamonu University Journal of Forestry Faculty, 19(3), 299-309. https://doi.org/10.17475/kastorman.662581
AMA Uğurlu Bayarslan A. Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome. Kastamonu University Journal of Forestry Faculty. December 2019;19(3):299-309. doi:10.17475/kastorman.662581
Chicago Uğurlu Bayarslan, Aslı. “Identification and Characterization of LEA Genes in Ash Tree (Fraxinus Excelsior) Genome”. Kastamonu University Journal of Forestry Faculty 19, no. 3 (December 2019): 299-309. https://doi.org/10.17475/kastorman.662581.
EndNote Uğurlu Bayarslan A (December 1, 2019) Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome. Kastamonu University Journal of Forestry Faculty 19 3 299–309.
IEEE A. Uğurlu Bayarslan, “Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome”, Kastamonu University Journal of Forestry Faculty, vol. 19, no. 3, pp. 299–309, 2019, doi: 10.17475/kastorman.662581.
ISNAD Uğurlu Bayarslan, Aslı. “Identification and Characterization of LEA Genes in Ash Tree (Fraxinus Excelsior) Genome”. Kastamonu University Journal of Forestry Faculty 19/3 (December 2019), 299-309. https://doi.org/10.17475/kastorman.662581.
JAMA Uğurlu Bayarslan A. Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome. Kastamonu University Journal of Forestry Faculty. 2019;19:299–309.
MLA Uğurlu Bayarslan, Aslı. “Identification and Characterization of LEA Genes in Ash Tree (Fraxinus Excelsior) Genome”. Kastamonu University Journal of Forestry Faculty, vol. 19, no. 3, 2019, pp. 299-0, doi:10.17475/kastorman.662581.
Vancouver Uğurlu Bayarslan A. Identification and Characterization of LEA Genes in Ash Tree (Fraxinus excelsior) Genome. Kastamonu University Journal of Forestry Faculty. 2019;19(3):299-30.

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