Araştırma Makalesi
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In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L.

Yıl 2018, Cilt: 5 Sayı: 1, 31 - 39, 28.02.2018
https://doi.org/10.19159/tutad.336202

Öz

Common bean is an important legume that grown
and consumed as animal feed and for human nutrition. It is also an important
source of protein in developing countries. Transposable elements (TEs)
constitute a large part of the genome in various eukaryotic species. TE was
described as garbage DNA by researchers for a long time. Recently, it has been
found that TEs can move near stress response genes and they have known effects
on plant resistance to diverse stresses. With the acquisition of common bean
genome sequence, one of the next step
is
to annotate the genome and define the functional DNA elements. TEs are the most
abundant genetic elements of plant genomes and have an important impact on
genome stress evolution and genetic variation. So, it is important to determine
TEs in the common bean genome. In the
current
study, genome-wide transposon annotation and definition were achieved in root
and leaf tissues of common bean under salt stress. Homology and sequence
structure-based methods were used. Tont2-I-Copia and Copia-39 Copia
retrotransposons were found to be more in
salt-treated
roots and
leaves respectively. As a
result of the analysis, we found TEs number ranging from 46 to 50 belonging to
about twenty different plants. Gene ontology analysis of transposon sequences
brought the light on diverse important pathways related to abiotic stress
conditions.

Kaynakça

  • Anonymous, 2017. VENNY, An Interactive Tool for Comparing Lists with Venn Diagrams BioinfoGP, CNB-CSIC by Juan C. Oliveros. (http://bioinfogp.cnb.csic.es/tools/venny/), (Date of access: 06.07.2017).
  • Beguiristain, T., Grandbastien, M.A., Puigdomènech, P., Casacuberta, J.M., 2001. Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiology, 127(1): 212-221.
  • Biémont, C., 2010. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics, 186(4): 1085-1093.
  • Bitocchi, E., Nanni, L., Bellucci, E., Rossi, M., Giardini, A., Zeuli, P.S., Logozzo, G., Stougaard, J., McClean, P., Attene, G., 2012. Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proceedings of the National Academy of Sciences, 109(14): E788-E796.
  • Blair, M.W., Hurtado, N., Chavarro, C.M., Muñoz-Torres, M.C., Giraldo, M.C., Pedraza, F., Tomkins, J., Wing, R., 2011. Gene-based SSR markers for common bean (Phaseolus vulgaris L.) derived from root and leaf tissue ESTs: an integration of the BMc series. BMC Plant Biology, 11(1): 50-60.
  • Brauc, S., De Vooght, E., Claeys, M., Höfte, M., Angenon, G., 2011. Influence of over-expression of cytosolic aspartate aminotransferase on amino acid metabolism and defense responses against Botrytis cinerea infection in Arabidopsis thaliana. Journal of Plant Physiology, 168(15): 1813-1819.
  • Capy, P., Gasperi, G., Biémont, C., Bazin, C., 2000. Stress and transposable elements: co‐evolution or useful parasites? Heredity, 85(2): 101-106.
  • Cavrak, V.V., Lettner, N., Jamge, S., Kosarewicz, A., Bayer, L.M., Scheid, O.M., 2014. How a retrotransposon exploits the plant's heat stress response for its activation. PLoS Genetics, 10(1): e1004115.
  • Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M., Robles, M., 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18): 3674-3676.
  • Cowley, M., Oakey, R.J., 2013. Transposable elements re-wire and fine-tune the transcriptome. PLoS genetics, 9(1): e1003234.
  • De Souza, F.S., Franchini, L.F., Rubinstein, M., 2013. Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Molecular Biology and Evolution, 30(6): 1239-1251.
  • Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E., Ecker, J.R., 2012. Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences, 109(32): E2183-E2191.
  • Eichten, S.R., Ellis, N.A., Makarevitch, I., Yeh, C.-T., Gent, J.I., Guo, L., McGinnis, K.M., Zhang, X., Schnable, P.S., Vaughn, M.W., 2012. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genetics, 8(12): e1003127.
  • Feschotte, C., 2008. The contribution of transposable elements to the evolution of regulatory networks. Nature Reviews Genetics, 9(5): 397.
  • Feschotte, C., Swamy, L., Wessler, S.R., 2003. Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics, 163(2): 747-758.
  • Gao, S., Liu, K.-T., Chung, T.-W., Chen, F., 2013. The effects of NaCl stress on Jatropha cotyledon growth and nitrogen metabolism. Journal of Soil Science and Plant Nutrition, 13(1): 99-113.
  • Grandbastien, M.A., Lucas, H., More, J.B., Mhiri, C., Vernhettes, S., Casacuberta, J.M., 1997. The expression of the tobacco Tnt1 is linked to the plant defense responses. Genetica, 100(1):241-252.
  • Grandbastien, M.-A., 1998. Activation of plant retrotransposons under stress conditions. Trends in Plant Science, 3(5): 181-187.
  • Guo, Y., Singh, P.K., Levin, H.L., 2015. A long terminal repeat retrotransposon of Schizosaccharomyces japonicus integrates upstream of RNA pol III transcribed genes. Mobile DNA, 6(1): 19-26.
  • Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., 2013. De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nature Protocols, 8(8): 50-69.
  • Hiz, M.C., Canher, B., Niron, H., Turet, M., 2014. Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PloS One, 9(3): e92598.
  • Hollister, J.D., Gaut, B.S., 2009. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Research, 19(8): 1419-1428.
  • Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., Paszkowski, J., 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature, 472 (7341): 115-124
  • Ito, H., Yoshida, T., Tsukahara, S., Kawabe, A., 2013. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene, 518(2): 256-261.
  • Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O., Walichiewicz, J., 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research, 110 (1):462-467.
  • Li, R., Hsieh, C.-L., Young, A., Zhang, Z., Ren, X., Zhao, Z., 2015. Illumina synthetic long read sequencing allows recovery of missing sequences even in the “finished” C. elegans genome. Scientific Reports, 5: 50-65.
  • Li, X., Kong, Y., Zhao, Q.-Y., Li, Y.-Y., Hao, P., 2016. De novo assembly of transcriptome from next-generation sequencing data. Quantitative Biology, 4(2): 94-105.
  • Lin, J.-Y., Stupar, R.M., Hans, C., Hyten, D.L., Jackson, S.A., 2010. Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. The Plant Cell, 22(8): 2545-2561.
  • Makarevitch, I., Waters, A.J., West, P.T., Stitzer, M., Hirsch, C.N., Ross-Ibarra, J., Springer, N.M., 2015. Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genetics, 11(1): e1004915.
  • McClean, P.E., Mamidi, S., McConnell, M., Chikara, S., Lee, R., 2010. Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics, 11(1): 184-194.
  • McClintock, B., 1956. Controlling elements and the gene, Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, 21: 197-216.
  • McClintock, B., 1963. Further studies of gene-control systems in maize. Carnegie Institution Washington Year Book, 62: 486-493.
  • McClintock, B., 1984. The significance of responses of the genome to challenge. Science, 4676(226): 792-801.
  • Nam, M.H., Huh, S.M., Kim, K.M., Park, W.W., Seo, J.B., Cho, K., Kim, D.Y., Kim, B.G., Yoon, I.I., 2012. Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteome Science, 10(1): 25-44.
  • Pecinka, A., Dinh, H.Q., Baubec, T., Rosa, M., Lettner, N., Scheid, O.M., 2010. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. The Plant Cell, 22(9): 3118-3129.
  • Ramanjulu, S., Veeranjaneyulu, K., Sudhakar, C., 1994. Short-term shifts in nitrogen metabolism in mulberry Morus alba under salt shock. Phytochemistry, 37(4): 991-995.
  • Sigmaz, B., Agar, G., Arslan, E., Aydin, M., Taspinar, M.S., 2015. The role of the putrescine against the long terminal repeat (LTR) retrotransposon polymorphism induced by salinity stress in Triticum aestivum. Acta Physiologiae Plantarum, 37(11): 251-259.
  • Weil, C., Wessler, S., 1990. The effects of plant transposable element insertion on transcription initiation and RNA processing. Annual Review of Plant Biology, 41(1): 527-552.
  • Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J. L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., 2007. A unified classification system for eukaryotic transposable elements. Nature Reviews Genetics, 8(12): 973-982.
  • Yasuda, K., Ito, M., Sugita, T., Tsukiyama, T., Saito, H., Naito, K., Teraishi, M., Tanisaka, T., Okumoto, Y., 2013. Utilization of transposable element mPing as a novel genetic tool for modification of the stress response in rice. Molecular Breeding, 32(3): 505-516.
  • Zhang, F., Zhu, G., Du, L., Shang, X., Cheng, C., Yang, B., Hu, Y., Cai, C., Guo, W., 2016. Genetic regulation of salt stress tolerance revealed by RNA-Seq in cotton diploid wild species, Gossypium davidsonii. Scientific Reports, 6: 1-15.

In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L.

Yıl 2018, Cilt: 5 Sayı: 1, 31 - 39, 28.02.2018
https://doi.org/10.19159/tutad.336202

Öz

Common bean is an important legume that grown and consumed as animal feed and for human nutrition. It is also an important source of protein in developing countries. Transposable elements (TEs) constitute a large part of the genome in various eukaryotic species. TE was described as garbage DNA by researchers for a long time. Recently, it has been found that TEs can move near stress response genes and they have known effects on plant resistance to diverse stresses. With the acquisition of common bean genome sequence, one of the next step is to annotate the genome and define the functional DNA elements. TEs are the most abundant genetic elements of plant genomes and have an important impact on genome stress evolution and genetic variation. So, it is important to determine TEs in the common bean genome. In the current study, genome-wide transposon annotation and definition were achieved in root and leaf tissues of common bean under salt stress. Homology and sequence structure-based methods were used. Tont2-I-Copia and Copia-39 Copia retrotransposons were found to be more in salt-treated roots and leaves respectively. As a result of the analysis, we found TEs number ranging from 46 to 50 belonging to about twenty different plants. Gene ontology analysis of transposon sequences brought the light on diverse important pathways related to abiotic stress conditions.

Kaynakça

  • Anonymous, 2017. VENNY, An Interactive Tool for Comparing Lists with Venn Diagrams BioinfoGP, CNB-CSIC by Juan C. Oliveros. (http://bioinfogp.cnb.csic.es/tools/venny/), (Date of access: 06.07.2017).
  • Beguiristain, T., Grandbastien, M.A., Puigdomènech, P., Casacuberta, J.M., 2001. Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiology, 127(1): 212-221.
  • Biémont, C., 2010. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics, 186(4): 1085-1093.
  • Bitocchi, E., Nanni, L., Bellucci, E., Rossi, M., Giardini, A., Zeuli, P.S., Logozzo, G., Stougaard, J., McClean, P., Attene, G., 2012. Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proceedings of the National Academy of Sciences, 109(14): E788-E796.
  • Blair, M.W., Hurtado, N., Chavarro, C.M., Muñoz-Torres, M.C., Giraldo, M.C., Pedraza, F., Tomkins, J., Wing, R., 2011. Gene-based SSR markers for common bean (Phaseolus vulgaris L.) derived from root and leaf tissue ESTs: an integration of the BMc series. BMC Plant Biology, 11(1): 50-60.
  • Brauc, S., De Vooght, E., Claeys, M., Höfte, M., Angenon, G., 2011. Influence of over-expression of cytosolic aspartate aminotransferase on amino acid metabolism and defense responses against Botrytis cinerea infection in Arabidopsis thaliana. Journal of Plant Physiology, 168(15): 1813-1819.
  • Capy, P., Gasperi, G., Biémont, C., Bazin, C., 2000. Stress and transposable elements: co‐evolution or useful parasites? Heredity, 85(2): 101-106.
  • Cavrak, V.V., Lettner, N., Jamge, S., Kosarewicz, A., Bayer, L.M., Scheid, O.M., 2014. How a retrotransposon exploits the plant's heat stress response for its activation. PLoS Genetics, 10(1): e1004115.
  • Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M., Robles, M., 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18): 3674-3676.
  • Cowley, M., Oakey, R.J., 2013. Transposable elements re-wire and fine-tune the transcriptome. PLoS genetics, 9(1): e1003234.
  • De Souza, F.S., Franchini, L.F., Rubinstein, M., 2013. Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Molecular Biology and Evolution, 30(6): 1239-1251.
  • Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E., Ecker, J.R., 2012. Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences, 109(32): E2183-E2191.
  • Eichten, S.R., Ellis, N.A., Makarevitch, I., Yeh, C.-T., Gent, J.I., Guo, L., McGinnis, K.M., Zhang, X., Schnable, P.S., Vaughn, M.W., 2012. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genetics, 8(12): e1003127.
  • Feschotte, C., 2008. The contribution of transposable elements to the evolution of regulatory networks. Nature Reviews Genetics, 9(5): 397.
  • Feschotte, C., Swamy, L., Wessler, S.R., 2003. Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics, 163(2): 747-758.
  • Gao, S., Liu, K.-T., Chung, T.-W., Chen, F., 2013. The effects of NaCl stress on Jatropha cotyledon growth and nitrogen metabolism. Journal of Soil Science and Plant Nutrition, 13(1): 99-113.
  • Grandbastien, M.A., Lucas, H., More, J.B., Mhiri, C., Vernhettes, S., Casacuberta, J.M., 1997. The expression of the tobacco Tnt1 is linked to the plant defense responses. Genetica, 100(1):241-252.
  • Grandbastien, M.-A., 1998. Activation of plant retrotransposons under stress conditions. Trends in Plant Science, 3(5): 181-187.
  • Guo, Y., Singh, P.K., Levin, H.L., 2015. A long terminal repeat retrotransposon of Schizosaccharomyces japonicus integrates upstream of RNA pol III transcribed genes. Mobile DNA, 6(1): 19-26.
  • Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., 2013. De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nature Protocols, 8(8): 50-69.
  • Hiz, M.C., Canher, B., Niron, H., Turet, M., 2014. Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PloS One, 9(3): e92598.
  • Hollister, J.D., Gaut, B.S., 2009. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Research, 19(8): 1419-1428.
  • Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., Paszkowski, J., 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature, 472 (7341): 115-124
  • Ito, H., Yoshida, T., Tsukahara, S., Kawabe, A., 2013. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene, 518(2): 256-261.
  • Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O., Walichiewicz, J., 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research, 110 (1):462-467.
  • Li, R., Hsieh, C.-L., Young, A., Zhang, Z., Ren, X., Zhao, Z., 2015. Illumina synthetic long read sequencing allows recovery of missing sequences even in the “finished” C. elegans genome. Scientific Reports, 5: 50-65.
  • Li, X., Kong, Y., Zhao, Q.-Y., Li, Y.-Y., Hao, P., 2016. De novo assembly of transcriptome from next-generation sequencing data. Quantitative Biology, 4(2): 94-105.
  • Lin, J.-Y., Stupar, R.M., Hans, C., Hyten, D.L., Jackson, S.A., 2010. Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. The Plant Cell, 22(8): 2545-2561.
  • Makarevitch, I., Waters, A.J., West, P.T., Stitzer, M., Hirsch, C.N., Ross-Ibarra, J., Springer, N.M., 2015. Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genetics, 11(1): e1004915.
  • McClean, P.E., Mamidi, S., McConnell, M., Chikara, S., Lee, R., 2010. Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics, 11(1): 184-194.
  • McClintock, B., 1956. Controlling elements and the gene, Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, 21: 197-216.
  • McClintock, B., 1963. Further studies of gene-control systems in maize. Carnegie Institution Washington Year Book, 62: 486-493.
  • McClintock, B., 1984. The significance of responses of the genome to challenge. Science, 4676(226): 792-801.
  • Nam, M.H., Huh, S.M., Kim, K.M., Park, W.W., Seo, J.B., Cho, K., Kim, D.Y., Kim, B.G., Yoon, I.I., 2012. Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteome Science, 10(1): 25-44.
  • Pecinka, A., Dinh, H.Q., Baubec, T., Rosa, M., Lettner, N., Scheid, O.M., 2010. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. The Plant Cell, 22(9): 3118-3129.
  • Ramanjulu, S., Veeranjaneyulu, K., Sudhakar, C., 1994. Short-term shifts in nitrogen metabolism in mulberry Morus alba under salt shock. Phytochemistry, 37(4): 991-995.
  • Sigmaz, B., Agar, G., Arslan, E., Aydin, M., Taspinar, M.S., 2015. The role of the putrescine against the long terminal repeat (LTR) retrotransposon polymorphism induced by salinity stress in Triticum aestivum. Acta Physiologiae Plantarum, 37(11): 251-259.
  • Weil, C., Wessler, S., 1990. The effects of plant transposable element insertion on transcription initiation and RNA processing. Annual Review of Plant Biology, 41(1): 527-552.
  • Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J. L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., 2007. A unified classification system for eukaryotic transposable elements. Nature Reviews Genetics, 8(12): 973-982.
  • Yasuda, K., Ito, M., Sugita, T., Tsukiyama, T., Saito, H., Naito, K., Teraishi, M., Tanisaka, T., Okumoto, Y., 2013. Utilization of transposable element mPing as a novel genetic tool for modification of the stress response in rice. Molecular Breeding, 32(3): 505-516.
  • Zhang, F., Zhu, G., Du, L., Shang, X., Cheng, C., Yang, B., Hu, Y., Cai, C., Guo, W., 2016. Genetic regulation of salt stress tolerance revealed by RNA-Seq in cotton diploid wild species, Gossypium davidsonii. Scientific Reports, 6: 1-15.
Toplam 41 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm Araştırma Makalesi / Research Article
Yazarlar

Behcet İnal 0000-0003-2215-2710

Yayımlanma Tarihi 28 Şubat 2018
Yayımlandığı Sayı Yıl 2018 Cilt: 5 Sayı: 1

Kaynak Göster

APA İnal, B. (2018). In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L. Türkiye Tarımsal Araştırmalar Dergisi, 5(1), 31-39. https://doi.org/10.19159/tutad.336202
AMA İnal B. In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L. TÜTAD. Şubat 2018;5(1):31-39. doi:10.19159/tutad.336202
Chicago İnal, Behcet. “In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus Vulgaris L”. Türkiye Tarımsal Araştırmalar Dergisi 5, sy. 1 (Şubat 2018): 31-39. https://doi.org/10.19159/tutad.336202.
EndNote İnal B (01 Şubat 2018) In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L. Türkiye Tarımsal Araştırmalar Dergisi 5 1 31–39.
IEEE B. İnal, “In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L”., TÜTAD, c. 5, sy. 1, ss. 31–39, 2018, doi: 10.19159/tutad.336202.
ISNAD İnal, Behcet. “In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus Vulgaris L”. Türkiye Tarımsal Araştırmalar Dergisi 5/1 (Şubat 2018), 31-39. https://doi.org/10.19159/tutad.336202.
JAMA İnal B. In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L. TÜTAD. 2018;5:31–39.
MLA İnal, Behcet. “In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus Vulgaris L”. Türkiye Tarımsal Araştırmalar Dergisi, c. 5, sy. 1, 2018, ss. 31-39, doi:10.19159/tutad.336202.
Vancouver İnal B. In Silico Analysis of Mobilome Response to Salt Stress in Phaseolus vulgaris L. TÜTAD. 2018;5(1):31-9.

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