Issue
Differential expression of 3β-HSD and mlncRNAs in response to abiotic stresses in Digitalis nervosa
Corresponding Author(s) : Asad Maroufi
Cellular and Molecular Biology,
Vol. 64 No. 14: Issue 14
Abstract
Digitalis nervosa is an important medicinal plant species belonging to the family of Scrophulariaceae that has the potential to be used for heart failure. 3β-hydroxysteroid dehydrogenase (3β-HSD) is a key gene in the biosynthesis of cardenolides for making digitalis effective compounds, hence identification of this gene is important for genetic engineering purposes towards increasing the yield of cardiac glycosides. In addition, mRNA-like non-coding RNAs (mlncRNAs), a class of long non coding RNAs, play key roles in various biological processes and may affect cardenolides pathway in digitalis plants. In the present work, full sequence of 3β-HSD was isolated from Digitalis nervosa. Gene expression patterns of 3β-HSD along with three mlncRNAs including mlncRNA23, mlncRNA28 and mlncRNA30 were studied and the results indicated that they are differentially expressed in different tissues including roots, stems and leaves, with the highest expression levels in leaves. Moreover, the transcript levels of these genes affected by the cold and drought stresses. The results obtained from the present study is important in order to understand the potential role of mlncRNAs in digitalis plants, especially in response to abiotic stresses.
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- Adib, A., Ghafghazi, T., 1991. Basic and clinical pharmacognosy, Alborz Press, Tehran.
- Agrawal, A.A., Petschenka, G., Bingham, R.A., Weber, M.G., Rasmann, S., 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant herbivore interactions. New Phytologist. 194, 28-45.
- Azadbakht, M., Ghasemi Dehkordi, N., 2001. Identification of cardiac glycosides of Iranian Digitalis species by HPLC. The Journal of Mazandaran University of Medical Sciences. 11 (31), 25-31.
- Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., d'Aubenton-Carafa, Y., Hirsch, J., Maizel, A., Mallory, A., Lucas, A., Deragon, J.M., Vaucheret, H., Thermes, C., Crespi, M, 2009. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 19(1), 57-69.
- Brauchler, C., Meimberg, H., Heubl, G., 2004. Molecular phylogeny of the genera Digitalis L. and Isoplexis (Lindley) Loudon (Veronicaceae) based on ITS and trnL-F sequences. Plant. Syst. Evol. 248, 111-128.
- Chen, M., Wang, C.L., Bao, H., Chen, H., Wang, Y.W., 2016. Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency. Mol Gen Genomics. 291(4), 1663-80.
- Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T., and Luan, S., 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129, 661-677.
- Chung, P.J., Jung, H., Jeong, D.H., Ha, S.H., Choi, Y.D., Kim, J.K., 2016. Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genomics. 17, 563.
- Clemente, E.S., Müller-Uri, F., Nebauer, S.G., Segura, J., Kreis, W., Arrillaga, I., 2011. Digitalis. In: Kole C, ed. Wild Crop Relatives: genomic and breeding Resources, Plantation and ornamental Crops. Berlin, Heidelberg, Springer.
- Ernst, M., Padua, R. M., Herl, V., Müller-Uri, F., Kreis., W., 2010. Expression of 3β"HSD and P5βR, Genes Respectively Coding for Δ5-3β-Hydroxysteroid Dehydrogenase and Progesterone 5β"Reductase in Leaves and Cell Cultures of Digitalis lanata. EHRH. Planta Med. 76(9), 923-927.
- Feng S.J, Zhang, X.D., Liu, X.S., Tan, S.K., Chu, S.S., Meng, J.G., Zhao K.X., Zhenga, J.F., Yang, Z.M., 2016. Characterization of long non-coding RNAs involved in cadmium toxic response in Brassica napus. RSC Advances. DOI:10.1039/C6RA05459E
- Ferdous, J., Hussain, S.S., Shi, B.J., 2015. Role of microRNAs in plant drought tolerance. Plant Biotechnol J. 13(3), 293-305.
- Finsterbusch, A., Lindemann, P., Grimm, R., Eckerskorn, C., Luckner, M., 1999. Delta (5)-3betahydroxysteroid dehydrogenase from Digitalis lanata Ehrh. - a multifunctional enzyme in steroid metabolism? Planta. 209(4), 478-86.
- Gartner, D. E., Seitz, H.U., 1990. A stereospecific enzyme of the putative biosynthetic pathway of cardenolides. Characterization of progesterone 5β-reductase from leaves of Digitalis purpurea L. FEBS Lett. 271, 239-242.
- Hauptman, P.J., Garg, R., Kelly, R.A., 1999. Cardiac glycosides in the next millennium. Prog Cardiovasc Dis. 41, 247-254.
- Herl, V., Fischer, G., Müller-Uri, F., Kreis, W., 2006. Molecular cloning and heterologous expression of progesterone 5β-reductase (P5βR) from Digitalis lanata EHRH. Phytochem. 67, 225–223.
- Herl, V., Frankenstein, J., Meitinger, N., Müller-Uri, F., Kreis, W., 2007. A (5)-3 beta-hydroxysteroid dehydrogenase (3βHSD) from Digitalis lanata. Heterologous expression and characterisation of the recombinant enzyme. Planta Med. 73, 704-710.
- Hood, W.B. Jr, Dans, A.L., Guyatt, G.H., Jaeschke, R., McMurray, J.J., 2014. Digitalis for treatment of heart failure in patients in sinus rhythm. Cochrane Database Syst Rev. 28, 4.
- Jia, H., Osak, M., Bogu, G.K., Stanton, L.W., Johnson, R., Lipovich, L., 2010. Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA. 16, 1478-1487.
- Jover-Gil, S., Candela, H., Ponce, M., 2005. Plant microRNAs and development. Int. J. Dev. Biol. 49, 733.
- Khraiwesh, B., Zhu, J.K., Zhu, J., 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta. 1819(2), 137-48.
- Kim, E.D., Sung, S., 2012. Long noncoding RNA: unveiling hidden layer of gene regulatory networks, Trends Plant Sci. 17(1), 16-21.
- Kreis, W., Müller-Uri, F., 2010. Biochemistry of sterols, cardiac glycosides, brassinosteroids, phytoecdysteroids and steroid saponins. In: M. Wink, (ed.) Biochemistry of Plant Secondary Metabolism. Annual Plant Reviews. CRC Press, Sheffield.
- Kreis, W., Müller-Ur, F., 2012. "Cardenolide aglycone formation in Digitalis,” in Isoprenoid Synthesis in Plants and Microorganisms, ed T. J. Bach, New York, Springer.
- Liu, J., Jung, C., Xu, J., Wang, H., Deng, S., Bernad, L., Arenas-Huertero, C., Chua, N.H., 2012. Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell. 24 (11), 4333-4345.
- Morris, K.V., Mattick, J.S., 2014. The rise of regulatory RNA. Nat Rev Genet. 15, 423-437.
- Munkert, J., Ernst M., Müller-Uri F., Kreis, W., 2014. Identification and stress-induced expression of three 3β-hydroxysteroid dehydrogenases from Erysimum crepidifolium Rchb. and their putative role in cardenolide biosynthesis. Phytochemistry. 100, 26-33.
- Paneru, B., Al-Tobasei, R., Palti, Y., Wiens, G.D., Salem, M., 2016. Differential expression of long non-coding RNAs in three genetic lines of rainbow trout in response to infection with Flavobacterium psychrophilum. Sci Rep. 6, 1-14.
- Pandey, A., Swarnkar, V., Pandey, T., Srivastava, P., Kanojiya S., Mishra, D.K., Tripathi, V., 2016. Transcriptome and metabolite analysis reveal candidate genes of the cardiac glycoside biosynthetic pathway from Calotropis procera. Sci Rep. 6, 34464.
- Perez-Bermudez, P., Moya García, A.A., Tuñon, I., Gavidia, I., 2010. Digitalis purpurea P5βR2, encoding steroid 5β-reductase, is a novel defense-related gene involved in cardenolide biosynthesis. New Phytol. 185, 687-700.
- Ponting, C.P., Oliver, P.L., Reik, W., 2009. Evolution and functions of long noncoding RNAs. Cell. 136, 629-641.
- Rechinger, K.H., 1979. Flora Iranica Austria: Akademiche Druk-u. 147, 169-170.
- Redrup, L., Branco, M.R., Perdeaux, E.R., Krueger, C., Lewis, A., Santos, F., Nagano, T., Cobb, B.S., Fraser, P., Reik, W., 2009. The long noncoding RNA Kcnq1ot1 organizes a lineage-specific nuclear domain for epigenetic gene silencing. Development. 136, 525-530.
- Roudbaraki, S. J., Nori-Shargh, D., 2016. The volatile constituent analysis of Digitalis nervosa Steud. & Hochst. ex Benth. from Iran. Russ Chem Bull. 65, 1148.
- Rymarquis, L.A., Kastenmayer, J.P., Huttenhofer, A.G., Green P.J., 2008. Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci. 13, 329-334.
- Sales, E., Müller-Uri F., Nebauer S.G., Segura J., Kreis W., Arrillaga I., 2011. Digitalis. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, plantation and ornamental crops. Springer, Berlin.
- Sunkar, R, Li, Y.F., Jagadeeswaran, G., 2012. Functions of microRNAs in plant stress responses. Trends Plant Sci. 17(4), 196-203.
- Thompson, J.D., Higgins, D.G., and Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
- Todaka, D., Nakashima, K., Shinozaki, K., Yamaguchi-Shinozaki, K., 2012. Towards understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice. 5, 1-9.
- Tran, T.T., Zhou, F., Marshburn, S., Stead, M., Kushner, S.R., Xu, Y., 2009. De novo computational prediction of non-coding RNA genes in prokaryotic genomes. Bioinformatics. 25, 2897-2905.
- Voss, B., Georg, J., Schon, V., Ude, S., Hess, W.R., 2009. Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics. 10,123.
- Watanabe, K.A., Ringler, P., Gu, L.K., Shen, Q.X.J., 2014. RNA-sequencing reveals previously unannotated protein- and microRNA-coding genes expressed in aleurone cells of rice seeds. Genomics. 103, 122-134.
- Wang, M., Wu, B., Chen, C., Lu, S., 2015. Identification of Panax ginseng mRNA-like non-coding RNAs and validation of a mighty one regulating multiple metabolic pathways. J. Integr. Plant Biol. 57, 254-268.
- Wang T., Liu M., Zhao, M., Chen, R., Zhang, W., 2015. Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol. 15, 131.
- Warren, B., 2005. Digitalis purpurea. Am J Cardiol. 95(4), 544.
- Wen, J., Parker, B.J., Weiller, G.F., 2007. In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol. 7, 485-505.
- Wirth, S., Crespi, M., 2009. Non-protein coding RNAs, a diverse class of gene regulators, and their action in plants. RNA Biology. 6(2), 161-164.
- Wu, B., Li, Y., Yan, H., Ma, Y., Luo, H., Yuan, L., Chen, S., and Lu, S., 2012. Comprehensive transcriptome analysis reveals novel genes involved in cardiac glycoside biosynthesis and mlncRNAs associated with secondary metabolism and stress response in Digitalis purpurea. BMC Genomics. 13, 15.
- Xin, M., Wang, Y., Yao, Y., Song, N., Hu, Z., Qin, D., Xie, C., Peng, H., Ni, Z., Sun, Q., 2011. Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol. 11, 61.
- Zhang, W., Han, Z.X., Guo, Q.L., Liu, Y., Zheng, Y.X., Wu, F.L., Jin, W.B., 2014. Identification of maize long non-coding RNAs responsive to drought stress. PLoS One. 9(6), e98958.
- Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., Luo, L., 2010. Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot. 61(15), 4157-68.
References
Adib, A., Ghafghazi, T., 1991. Basic and clinical pharmacognosy, Alborz Press, Tehran.
Agrawal, A.A., Petschenka, G., Bingham, R.A., Weber, M.G., Rasmann, S., 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant herbivore interactions. New Phytologist. 194, 28-45.
Azadbakht, M., Ghasemi Dehkordi, N., 2001. Identification of cardiac glycosides of Iranian Digitalis species by HPLC. The Journal of Mazandaran University of Medical Sciences. 11 (31), 25-31.
Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., d'Aubenton-Carafa, Y., Hirsch, J., Maizel, A., Mallory, A., Lucas, A., Deragon, J.M., Vaucheret, H., Thermes, C., Crespi, M, 2009. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 19(1), 57-69.
Brauchler, C., Meimberg, H., Heubl, G., 2004. Molecular phylogeny of the genera Digitalis L. and Isoplexis (Lindley) Loudon (Veronicaceae) based on ITS and trnL-F sequences. Plant. Syst. Evol. 248, 111-128.
Chen, M., Wang, C.L., Bao, H., Chen, H., Wang, Y.W., 2016. Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency. Mol Gen Genomics. 291(4), 1663-80.
Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T., and Luan, S., 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129, 661-677.
Chung, P.J., Jung, H., Jeong, D.H., Ha, S.H., Choi, Y.D., Kim, J.K., 2016. Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genomics. 17, 563.
Clemente, E.S., Müller-Uri, F., Nebauer, S.G., Segura, J., Kreis, W., Arrillaga, I., 2011. Digitalis. In: Kole C, ed. Wild Crop Relatives: genomic and breeding Resources, Plantation and ornamental Crops. Berlin, Heidelberg, Springer.
Ernst, M., Padua, R. M., Herl, V., Müller-Uri, F., Kreis., W., 2010. Expression of 3β"HSD and P5βR, Genes Respectively Coding for Δ5-3β-Hydroxysteroid Dehydrogenase and Progesterone 5β"Reductase in Leaves and Cell Cultures of Digitalis lanata. EHRH. Planta Med. 76(9), 923-927.
Feng S.J, Zhang, X.D., Liu, X.S., Tan, S.K., Chu, S.S., Meng, J.G., Zhao K.X., Zhenga, J.F., Yang, Z.M., 2016. Characterization of long non-coding RNAs involved in cadmium toxic response in Brassica napus. RSC Advances. DOI:10.1039/C6RA05459E
Ferdous, J., Hussain, S.S., Shi, B.J., 2015. Role of microRNAs in plant drought tolerance. Plant Biotechnol J. 13(3), 293-305.
Finsterbusch, A., Lindemann, P., Grimm, R., Eckerskorn, C., Luckner, M., 1999. Delta (5)-3betahydroxysteroid dehydrogenase from Digitalis lanata Ehrh. - a multifunctional enzyme in steroid metabolism? Planta. 209(4), 478-86.
Gartner, D. E., Seitz, H.U., 1990. A stereospecific enzyme of the putative biosynthetic pathway of cardenolides. Characterization of progesterone 5β-reductase from leaves of Digitalis purpurea L. FEBS Lett. 271, 239-242.
Hauptman, P.J., Garg, R., Kelly, R.A., 1999. Cardiac glycosides in the next millennium. Prog Cardiovasc Dis. 41, 247-254.
Herl, V., Fischer, G., Müller-Uri, F., Kreis, W., 2006. Molecular cloning and heterologous expression of progesterone 5β-reductase (P5βR) from Digitalis lanata EHRH. Phytochem. 67, 225–223.
Herl, V., Frankenstein, J., Meitinger, N., Müller-Uri, F., Kreis, W., 2007. A (5)-3 beta-hydroxysteroid dehydrogenase (3βHSD) from Digitalis lanata. Heterologous expression and characterisation of the recombinant enzyme. Planta Med. 73, 704-710.
Hood, W.B. Jr, Dans, A.L., Guyatt, G.H., Jaeschke, R., McMurray, J.J., 2014. Digitalis for treatment of heart failure in patients in sinus rhythm. Cochrane Database Syst Rev. 28, 4.
Jia, H., Osak, M., Bogu, G.K., Stanton, L.W., Johnson, R., Lipovich, L., 2010. Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA. 16, 1478-1487.
Jover-Gil, S., Candela, H., Ponce, M., 2005. Plant microRNAs and development. Int. J. Dev. Biol. 49, 733.
Khraiwesh, B., Zhu, J.K., Zhu, J., 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta. 1819(2), 137-48.
Kim, E.D., Sung, S., 2012. Long noncoding RNA: unveiling hidden layer of gene regulatory networks, Trends Plant Sci. 17(1), 16-21.
Kreis, W., Müller-Uri, F., 2010. Biochemistry of sterols, cardiac glycosides, brassinosteroids, phytoecdysteroids and steroid saponins. In: M. Wink, (ed.) Biochemistry of Plant Secondary Metabolism. Annual Plant Reviews. CRC Press, Sheffield.
Kreis, W., Müller-Ur, F., 2012. "Cardenolide aglycone formation in Digitalis,” in Isoprenoid Synthesis in Plants and Microorganisms, ed T. J. Bach, New York, Springer.
Liu, J., Jung, C., Xu, J., Wang, H., Deng, S., Bernad, L., Arenas-Huertero, C., Chua, N.H., 2012. Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell. 24 (11), 4333-4345.
Morris, K.V., Mattick, J.S., 2014. The rise of regulatory RNA. Nat Rev Genet. 15, 423-437.
Munkert, J., Ernst M., Müller-Uri F., Kreis, W., 2014. Identification and stress-induced expression of three 3β-hydroxysteroid dehydrogenases from Erysimum crepidifolium Rchb. and their putative role in cardenolide biosynthesis. Phytochemistry. 100, 26-33.
Paneru, B., Al-Tobasei, R., Palti, Y., Wiens, G.D., Salem, M., 2016. Differential expression of long non-coding RNAs in three genetic lines of rainbow trout in response to infection with Flavobacterium psychrophilum. Sci Rep. 6, 1-14.
Pandey, A., Swarnkar, V., Pandey, T., Srivastava, P., Kanojiya S., Mishra, D.K., Tripathi, V., 2016. Transcriptome and metabolite analysis reveal candidate genes of the cardiac glycoside biosynthetic pathway from Calotropis procera. Sci Rep. 6, 34464.
Perez-Bermudez, P., Moya García, A.A., Tuñon, I., Gavidia, I., 2010. Digitalis purpurea P5βR2, encoding steroid 5β-reductase, is a novel defense-related gene involved in cardenolide biosynthesis. New Phytol. 185, 687-700.
Ponting, C.P., Oliver, P.L., Reik, W., 2009. Evolution and functions of long noncoding RNAs. Cell. 136, 629-641.
Rechinger, K.H., 1979. Flora Iranica Austria: Akademiche Druk-u. 147, 169-170.
Redrup, L., Branco, M.R., Perdeaux, E.R., Krueger, C., Lewis, A., Santos, F., Nagano, T., Cobb, B.S., Fraser, P., Reik, W., 2009. The long noncoding RNA Kcnq1ot1 organizes a lineage-specific nuclear domain for epigenetic gene silencing. Development. 136, 525-530.
Roudbaraki, S. J., Nori-Shargh, D., 2016. The volatile constituent analysis of Digitalis nervosa Steud. & Hochst. ex Benth. from Iran. Russ Chem Bull. 65, 1148.
Rymarquis, L.A., Kastenmayer, J.P., Huttenhofer, A.G., Green P.J., 2008. Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci. 13, 329-334.
Sales, E., Müller-Uri F., Nebauer S.G., Segura J., Kreis W., Arrillaga I., 2011. Digitalis. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, plantation and ornamental crops. Springer, Berlin.
Sunkar, R, Li, Y.F., Jagadeeswaran, G., 2012. Functions of microRNAs in plant stress responses. Trends Plant Sci. 17(4), 196-203.
Thompson, J.D., Higgins, D.G., and Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
Todaka, D., Nakashima, K., Shinozaki, K., Yamaguchi-Shinozaki, K., 2012. Towards understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice. 5, 1-9.
Tran, T.T., Zhou, F., Marshburn, S., Stead, M., Kushner, S.R., Xu, Y., 2009. De novo computational prediction of non-coding RNA genes in prokaryotic genomes. Bioinformatics. 25, 2897-2905.
Voss, B., Georg, J., Schon, V., Ude, S., Hess, W.R., 2009. Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics. 10,123.
Watanabe, K.A., Ringler, P., Gu, L.K., Shen, Q.X.J., 2014. RNA-sequencing reveals previously unannotated protein- and microRNA-coding genes expressed in aleurone cells of rice seeds. Genomics. 103, 122-134.
Wang, M., Wu, B., Chen, C., Lu, S., 2015. Identification of Panax ginseng mRNA-like non-coding RNAs and validation of a mighty one regulating multiple metabolic pathways. J. Integr. Plant Biol. 57, 254-268.
Wang T., Liu M., Zhao, M., Chen, R., Zhang, W., 2015. Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol. 15, 131.
Warren, B., 2005. Digitalis purpurea. Am J Cardiol. 95(4), 544.
Wen, J., Parker, B.J., Weiller, G.F., 2007. In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol. 7, 485-505.
Wirth, S., Crespi, M., 2009. Non-protein coding RNAs, a diverse class of gene regulators, and their action in plants. RNA Biology. 6(2), 161-164.
Wu, B., Li, Y., Yan, H., Ma, Y., Luo, H., Yuan, L., Chen, S., and Lu, S., 2012. Comprehensive transcriptome analysis reveals novel genes involved in cardiac glycoside biosynthesis and mlncRNAs associated with secondary metabolism and stress response in Digitalis purpurea. BMC Genomics. 13, 15.
Xin, M., Wang, Y., Yao, Y., Song, N., Hu, Z., Qin, D., Xie, C., Peng, H., Ni, Z., Sun, Q., 2011. Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol. 11, 61.
Zhang, W., Han, Z.X., Guo, Q.L., Liu, Y., Zheng, Y.X., Wu, F.L., Jin, W.B., 2014. Identification of maize long non-coding RNAs responsive to drought stress. PLoS One. 9(6), e98958.
Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., Luo, L., 2010. Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot. 61(15), 4157-68.