Effect of drought stress on expression oftwo important miRNAs in anther of two different wheat genotypes in term of drought stress

Document Type : Research Paper

Authors

1 Ph.D. Student, Dept. of Agronomy and Plant Breeding, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

2 Assoc. Prof., Dept. of Agronomy and Plant Breeding, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

3 Assist. Prof.,Dept. of Agronomy and Plant Breeding, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

Abstract

A large amount of the world lands under the cultivation of wheat is under drought stress. In cereals, the reproductive stage is the most sensitive phase to drought stress. Despite the importance of drought stress in reproductive stage and its role in wheat yield reduction, the mechanisms involved in it have been less studied. In the present study, the expression of miR166 and miR167 in mature anthers of two tolerant (Dezfoul or D-10) and susceptible (Shiraz) wheat genotypes under drought conditions in reproductive stage was investigated. Stress tolerance index (STI) for grain number per spike, grain set and pollen viability was higher in tolerant genotype, Dezfoul, compared to susceptible genotype, Shiraz. Drought stress induced expression level of both miRNAs in both genotypes. The amount of miR166 increase in the susceptible genotype, Shiraz (over 14 times compared to the non-stress conditions) was about twice more than the tolerant genotype,Dezfoul (about 8 timesmore than the non-stress conditions). Under drought stress conditions, expression of miR167 in Dezfoulgenotype was more than two fold and in Shiraz genotype more than four timeshigher thanthe non-stress conditions. Both miR166 and miR167 regulate development of floral organs such as microspore development. In conclusion, the effect of drought stress on their expression changes can affect male sterility in wheat, and modifying the expression of these two miRNAscan lead to efficiency of pollen development and successful anther dehiscence which is rooted in signal transduction.

Keywords

References

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Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Functional Plant Biology 30: 271-280.##Liu, H. H., Tian, X., Li, Y. J., Wu, C. A. and Zheng, C. C. 2008. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836-843.##Liu, N., Wu, S., Van Houten, J., Wang, Y., Ding, B., Fei, Z., Clarke, T. H., Reed, J. W. and Van Der Knaap, E. 2014. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. Journal of Experimental Botany 65: 2507-2520.##Liu, X., Xu, T., Dong, X., Liu, Y., Liu, Z., Shi, Z., Wang, Y., Qi, M. and Li, T. 2016. The role of gibberellins and auxin on the tomato cell layers in pericarp via the expression of ARFs regulated by miRNAs in fruit set. Acta Physiologiae Plantarum 38: 77-88.##Luo, Y., Guo, Z. and Li, L. 2013. Evolutionary conservation of microRNA regulatory programs in plant flower development. Developmental Biology 380: 133-144.##Manavella, P. A., Dezar, C. A., Ariel, F. D., Drincovich, M. F. and Chan, R. L. 2008. The sunflower HD-Zip transcription factor HAHB4 is up-regulated in darkness, reducing the transcription of photosynthesis-related genes. Journal of Experimental Botany 59: 3143-3155.##Nonomura, K. I., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H. and Kurata, N. 2007. A germ cell–specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. The Plant Cell 19: 2583-2594.##Omidvar, V., Mohorianu, I., Dalmay, T. and Fellner, M. 2015. Identification of miRNAswith potential roles in regulation of anther development and malesterility in 7B-1 malesterile tomato mutant. BMC Genomics 16: 878-894.##Ribone, P. A., Capella, M. and Chan, R. L. 2015. Functional characterization of the homeodomain leucine zipper I transcription factor AtHB13 reveals a crucial role in Arabidopsis development. Journal of Experimental Botany 66: 5929-5943.##Ron, M., Saez, M. A., Williams, L. E., Fletcher, J. C. and McCormick, S. 2010. Proper regulation of a sperm-specific cis-nat-siRNA is essentialfor double fertilization in Arabidopsis. Genes and Development 24: 1010-1021.##Ru, P., Xu, L., Ma, H. and Huang, H. 2006. Plant fertility defects induced by the enhanced expression of microRNA167. Cell Research 16: 457-465.##Saba, J., Moghaddam, M., Ghasemi, K. and Nishabouri, M. 2010. Genetic properties of drought resistance indices. Journal of Agricultural Science and Technology 3: 43-49.##Schmittgen, T. D. and Livak, K. J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols3: 1101-1108.##Schommer, C., Palatnik, J. F., Aggarwal, P., Chételat, A., Cubas, P., Farmer, E. E., Nath, U. and Weigel, D. 2008. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biology 6: e230.##Sheehan, M. J. and Pawlowski, W. P. 2012. Imaging chromosome dynamics in meiosis in plants. Methods in Enzymology505:125-143.##Shriram, V., Kumar, V., Devarumath, R., Khare, T. S. and Wani, S. H. 2016. MicroRNAs as potential targets for abiotic stress tolerance in plants. Frontiers in Plant Science 7: 817-835.##Siddique, M., Hamid, A. and Islam, M. 2000. Drought stress effects on water relations of wheat. Botanical Bulletin of Academia Sinica 41: 35-39.##Song, G., Zhang, R., Zhang, S., Li, Y., Gao, J., Han, X., Chen, M., Wang, J., Li, W. and Li, G. 2017. Response of microRNAs to cold treatment in the young spikes of common wheat. BMC Genomics 18: 212-227.##Sundberg, E. and Østergaard, L. 2009. Distinct and dynamic auxin activities during reproductive development. Cold Spring Harbor Perspectives in Biology 1: a001628.##Sunkar, R. and Zhu, J. K. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell 16: 2001-2019.##Tabata, R., Ikezaki, M., Fujibe, T., Aida, M., Tian, C. E., Ueno, Y., Yamamoto, K. T., Machida, Y., Nakamura, K. and Ishiguro, S. 2009.Arabidopsis auxin response factor6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant and Cell Physiology 51: 164-175.##Tang, Z., Zhang, L., Xu, C., Yuan, S., Zhang, F., Zheng, Y. and Zhao, C. 2012. Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiology 159: 721-738.##Teotia, P. S., Mukherjee, S. K. and Mishra, N. S. 2008. Fine tuning of auxin signaling by miRNAs. Physiology and Molecular Biology of Plants 14: 81-90.##Tiwari, S. B., Hagen, G. and Guilfoyle, T. 2003. The roles of auxin response factor domains in auxin-responsive transcription. The Plant Cell 15: 533-543.##Twell, D. 2011. Male gametogenesis and germline specification in flowering plants. Sexual Plant Reproduction 24: 149-160.##Wang, J. C., Xu, H., Zhu, Y., Liu, Q. Q. and Cai, X. L. 2013. OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. Journal of Experimental Botany 64: 3453-3466.##Wei, M., Wei, H., Wu, M., Song, M., Zhang, J., Yu, J., Fan, S. and Yu, S. 2013. Comparative expression profiling of miRNA during anther development in genetic male sterile and wild type cotton. BMC Plant Biology 13: 66-80.##Wu, M.F., Tian, Q. and Reed, J. W. 2006.Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.##Xin, M., Wang, Y., Yao, Y., Xie, C., Peng, H., Ni, Z. and Sun, Q. 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biology 10: 123-134.##Yin, F., Gao, J., Liu, M., Qin, C., Zhang, W., Yang, A., Xia, M., Zhang, Z., Shen, Y. and Lin, H. 2014. Genome-wide analysis of water-stress-responsive microRNA expression profile in tobacco roots. Functional andIntegrative Genomics 14: 319-332.##Zare, S., Shobbar, Z. S. and Fotovat, R. 2016. Expression analysis of genes involved in the male sterility of wheat under drought stress during meiosis.Journal of Crop Biotechnology 13: 69-77. (In Persian with English Abstract).##Zhang, Q., Li, J., Sang, Y., Xing, S., Wu, Q. and Liu, X. 2015. Identification and characterization of microRNAs in Ginkgo Biloba var. Epiphylla Mak. PLoS One 10: e0127184.##Zhang, Y., Yin, Z., Feng, X. and Shen, F. 2013. Differential expression of microRNAs between 21A genetic male sterile line and its maintainer line in cotton (Gossypium hirsutum L.). Journal of Plant Studies 3: 13-27.##Zhu, H., Hu, F., Wang, R., Zhou, X., Sze, S. H., Liou, L. W., Barefoot, A., Dickman, M. and Zhang, X. 2011.ArabidopsisArgonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145: 242-256.
Akdogan, G., Tufekci, E. D., Uranbey, S. and Unver, T. 2016. miRNA-based drought regulation in wheat. Functional andIntegrative Genomics 16: 221-233.##Alexandratos, N. and Bruinsma, J. 2012. World agriculture towards 2030/2050: The 2012 revision, ESA Working Paper,FAO,Rome, Italy.##An, F. M., Hsiao, S. R. and Chan, M. T. 2011. Sequencing-based approaches reveal low ambient temperature-responsive and tissue-specific microRNAs in phalaenopsis orchid. PLoS One 6:e18937.##Ariel, F. D., Manavella, P. A., Dezar, C. A. and Chan, R. L. 2007. The true story of the HD-Zip family. Trends in Plant Science 12: 419-426.##Bakhshi, B., Fard, E. M., Gharechahi, J., Safarzadeh, M., Nikpay, N., Fotovat, R., Azimi, M. R. and Salekdeh, G. H. 2017. The contrasting microRNA content of a drought tolerant and a drought susceptible wheat cultivar. Journal of Plant Physiology 216: 35-43.##Barnabás, B., Jäger, K. and Fehér, A. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell andEnvironment 31: 11-38.##Cecchetti, V., Altamura, M. M., Falasca, G., Costantino, P. and Cardarelli, M. 2008. Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. The Plant Cell 20: 1760-1774.##Chhun, T., Aya, K., Asano, K., Yamamoto, E., Morinaka, Y., Watanabe, M., Kitano, H., Ashikari, M., Matsuoka, M. and Ueguchi-Tanaka, M. 2007. Gibberellin regulates pollen viability and pollen tube growth in rice. The Plant Cell19: 3876-3888.##Ding, Y., Tao, Y. and Zhu, C. 2013. Emerging roles of microRNAs in the mediation of drought stress response in plants. Journal of Experimental Botany 64: 3077-3086.##Dorion, S., Lalonde, S. and Saini, H. S. 1996. Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiology 111: 137-145.##FAO. 2016. Statistics: FAOSTAT agriculture. Food and Agriculture Organization. Retrieved September 20, 2018, from http://fao.org/crop/statistics.##Fard, E. M., Bakhshi, B., Farsi, M., Kakhki, A. M., Nikpay, N., Ebrahimi, M. A., Mardi, M. and Salekdeh, G. H. 2017. MicroRNAs regulate the main events in rice drought stress response by manipulating the water supply to shoots. Molecular Biosystems 13: 2289-2302.##Fotovat, R., Alikhani, M., Valizadeh, M., Mirzaei, M. and Salekdeh, G. H. 2017. A proteomics approach to discover drought tolerance proteins in wheat pollen grain at meiosis stage. Protein and Peptide Letters 24: 26-36.##Fujioka, T., Kaneko, F., Kazama, T., Suwabe, K., Suzuki, G., Makino, A., Mae, T., Endo, M., Kawagishi-Kobayashi, M. and Watanabe, M. 2008. Identification of small RNAs in late developmental stage of rice anthers. Genes andGenetic Systems 83: 281-284.##Grant-Downton, R., Hafidh, S., Twell, D. and Dickinson, H. G. 2009. Small RNA pathways are present and functional in the angiosperm male gametophyte. Molecular Plant 2: 500-512.##Huntzinger, E. and Izaurralde, E. 2011. Gene silencing by microRNAs: Contributions of translational repression and mRNA decay. Nature Reviews Genetics 12: 99-110.##Ji, L., Liu, X., Yan, J., Wang, W., Yumul, R. E., Kim, Y. J., Dinh, T. T., Liu, J., Cui, X. and Zheng, B. 2011. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genetics 7: e1001358.##Ji, X., Shiran,B., Wan, J., Lewis, D. C., Jenkins, C. L., Condon, A. G., Richards, R. A. and Dolferus, R. 2010. Importance of pre‐anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant, Cell and Environment 33: 926-942.##Jian-Chang, Y., Kai, L., Zhang, S. F., Xue-Ming, W., Zhi-Qin, W. and Li-Jun, L. 2008. Hormones in rice spikelets in responses to water stress during meiosis. Acta Agronomica Sinica 34: 111-118.##Jung, J. H. and Park, C. M. 2007. MIR166/165 genes exhibit dynamic expression patterns in regulating shootapical meristem and floral development in Arabidopsis. Planta 225: 1327-1338.##Kim, J., Jung, J. H., Reyes, J. L., Kim, Y. S., Kim, S. Y., Chung, K. S., Kim, J. A., Lee, M., Lee, Y. and Narry Kim, V. 2005. microRNA‐directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. The Plant Journal 42: 84-94.##Koonjul, P., Minhas, J., Nunes, C., Sheoran, I. and Saini, H. 2005. Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development inwater-stressed wheat. Journal of Experimental Botany 56: 179-190.##Krizek, B. A. 2011. Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) family. Journal of Experimental Botany
62: 3311-3319.##Lee, R. C., Feinbaum, R. L. and Ambros, V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.##Li, B., Qin, Y., Duan, H., Yin, W. and Xia, X. 2011. Genome-wide characterization of new anddrought stress responsive microRNAs in Populus euphratica. Journal of Experimental Botany 62: 3765-3779.##Li, Q. J., Xu, B., Chen, X. Y. and Wang, L. J. 2007. The effects of increased expression of an ArabidopsisHD-ZIPgeneonleafmorphogenesisandantherdehiscence.PlantScience173:567-576.##Li, Z. F., Zhang, Y. C. and Chen, Y. Q. 2015. miRNAs and lncRNAs in reproductive development. Plant Science 238: 46-52.##Lian, H., Li, X., Liu, Z. and He, Y. 2013. HYL1 is required for establishment of stamen architecture with four microsporangia in Arabidopsis. Journal of Experimental Botany 64: 3397-3410.##Liu, F., Andersen, M. N. and Jensen, C. R. 2003. Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Functional Plant Biology 30: 271-280.##Liu, H. H., Tian, X., Li, Y. J., Wu, C. A. and Zheng, C. C. 2008. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836-843.##Liu, N., Wu, S., Van Houten, J., Wang, Y., Ding, B., Fei, Z., Clarke, T. H., Reed, J. W. and Van Der Knaap, E. 2014. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. Journal of Experimental Botany 65: 2507-2520.##Liu, X., Xu, T., Dong, X., Liu, Y., Liu, Z., Shi, Z., Wang, Y., Qi, M. and Li, T. 2016. The role of gibberellins and auxin on the tomato cell layers in pericarp via the expression of ARFs regulated by miRNAs in fruit set. Acta Physiologiae Plantarum 38: 77-88.##Luo, Y., Guo, Z. and Li, L. 2013. Evolutionary conservation of microRNA regulatory programs in plant flower development. Developmental Biology 380: 133-144.##Manavella, P. A., Dezar, C. A., Ariel, F. D., Drincovich, M. F. and Chan, R. L. 2008. The sunflower HD-Zip transcription factor HAHB4 is up-regulated in darkness, reducing the transcription of photosynthesis-related genes. Journal of Experimental Botany 59: 3143-3155.##Nonomura, K. I., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H. and Kurata, N. 2007. A germ cell–specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. The Plant Cell 19: 2583-2594.##Omidvar, V., Mohorianu, I., Dalmay, T. and Fellner, M. 2015. Identification of miRNAswith potential roles in regulation of anther development and malesterility in 7B-1 malesterile tomato mutant. BMC Genomics 16: 878-894.##Ribone, P. A., Capella, M. and Chan, R. L. 2015. Functional characterization of the homeodomain leucine zipper I transcription factor AtHB13 reveals a crucial role in Arabidopsis development. Journal of Experimental Botany 66: 5929-5943.##Ron, M., Saez, M. A., Williams, L. E., Fletcher, J. C. and McCormick, S. 2010. Proper regulation of a sperm-specific cis-nat-siRNA is essentialfor double fertilization in Arabidopsis. Genes and Development 24: 1010-1021.##Ru, P., Xu, L., Ma, H. and Huang, H. 2006. Plant fertility defects induced by the enhanced expression of microRNA167. Cell Research 16: 457-465.##Saba, J., Moghaddam, M., Ghasemi, K. and Nishabouri, M. 2010. Genetic properties of drought resistance indices. Journal of Agricultural Science and Technology 3: 43-49.##Schmittgen, T. D. and Livak, K. J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols3: 1101-1108.##Schommer, C., Palatnik, J. F., Aggarwal, P., Chételat, A., Cubas, P., Farmer, E. E., Nath, U. and Weigel, D. 2008. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biology 6: e230.##Sheehan, M. J. and Pawlowski, W. P. 2012. Imaging chromosome dynamics in meiosis in plants. Methods in Enzymology505:125-143.##Shriram, V., Kumar, V., Devarumath, R., Khare, T. S. and Wani, S. H. 2016. MicroRNAs as potential targets for abiotic stress tolerance in plants. Frontiers in Plant Science 7: 817-835.##Siddique, M., Hamid, A. and Islam, M. 2000. Drought stress effects on water relations of wheat. Botanical Bulletin of Academia Sinica 41: 35-39.##Song, G., Zhang, R., Zhang, S., Li, Y., Gao, J., Han, X., Chen, M., Wang, J., Li, W. and Li, G. 2017. Response of microRNAs to cold treatment in the young spikes of common wheat. BMC Genomics 18: 212-227.##Sundberg, E. and Østergaard, L. 2009. Distinct and dynamic auxin activities during reproductive development. Cold Spring Harbor Perspectives in Biology 1: a001628.##Sunkar, R. and Zhu, J. K. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell 16: 2001-2019.##Tabata, R., Ikezaki, M., Fujibe, T., Aida, M., Tian, C. E., Ueno, Y., Yamamoto, K. T., Machida, Y., Nakamura, K. and Ishiguro, S. 2009.Arabidopsis auxin response factor6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant and Cell Physiology 51: 164-175.##Tang, Z., Zhang, L., Xu, C., Yuan, S., Zhang, F., Zheng, Y. and Zhao, C. 2012. Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiology 159: 721-738.##Teotia, P. S., Mukherjee, S. K. and Mishra, N. S. 2008. Fine tuning of auxin signaling by miRNAs. Physiology and Molecular Biology of Plants 14: 81-90.##Tiwari, S. B., Hagen, G. and Guilfoyle, T. 2003. The roles of auxin response factor domains in auxin-responsive transcription. The Plant Cell 15: 533-543.##Twell, D. 2011. Male gametogenesis and germline specification in flowering plants. Sexual Plant Reproduction 24: 149-160.##Wang, J. C., Xu, H., Zhu, Y., Liu, Q. Q. and Cai, X. L. 2013. OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. Journal of Experimental Botany 64: 3453-3466.##Wei, M., Wei, H., Wu, M., Song, M., Zhang, J., Yu, J., Fan, S. and Yu, S. 2013. Comparative expression profiling of miRNA during anther development in genetic male sterile and wild type cotton. BMC Plant Biology 13: 66-80.##Wu, M.F., Tian, Q. and Reed, J. W. 2006.Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.##Xin, M., Wang, Y., Yao, Y., Xie, C., Peng, H., Ni, Z. and Sun, Q. 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biology 10: 123-134.##Yin, F., Gao, J., Liu, M., Qin, C., Zhang, W., Yang, A., Xia, M., Zhang, Z., Shen, Y. and Lin, H. 2014. Genome-wide analysis of water-stress-responsive microRNA expression profile in tobacco roots. Functional andIntegrative Genomics 14: 319-332.##Zare, S., Shobbar, Z. S. and Fotovat, R. 2016. Expression analysis of genes involved in the male sterility of wheat under drought stress during meiosis.Journal of Crop Biotechnology 13: 69-77. (In Persian with English Abstract).##Zhang, Q., Li, J., Sang, Y., Xing, S., Wu, Q. and Liu, X. 2015. Identification and characterization of microRNAs in Ginkgo Biloba var. Epiphylla Mak. PLoS One 10: e0127184.##Zhang, Y., Yin, Z., Feng, X. and Shen, F. 2013. Differential expression of microRNAs between 21A genetic male sterile line and its maintainer line in cotton (Gossypium hirsutum L.). Journal of Plant Studies 3: 13-27.##Zhu, H., Hu, F., Wang, R., Zhou, X., Sze, S. H., Liou, L. 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Cereal Research
Volume 8, Issue 3
December 2018
Pages 359-369

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