Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Transcriptome Profiling and Characterization of Drought-Tolerant Potato Plant (Solanum tuberosum L.)

  • Moon, Ki-Beom (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Ahn, Dong-Joo (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Park, Ji-Sun (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Jung, Won Yong (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Cho, Hye Sun (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Kim, Hye-Ran (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Jeon, Jae-Heung (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Park, Youn-il (Department of Biological Sciences, Chungnam National University) ;
  • Kim, Hyun-Soon (Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology)
  • Received : 2018.07.23
  • Accepted : 2018.09.18
  • Published : 2018.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

Potato (Solanum tuberosum L.) is the third most important food crop, and breeding drought-tolerant varieties is vital research goal. However, detailed molecular mechanisms in response to drought stress in potatoes are not well known. In this study, we developed EMS-mutagenized potatoes that showed significant tolerance to drought stress compared to the wild-type (WT) 'Desiree' cultivar. In addition, changes to transcripts as a result of drought stress in WT and drought-tolerant (DR) plants were investigated by de novo assembly using the Illumina platform. One-week-old WT and DR plants were treated with -1.8 Mpa polyethylene glycol-8000, and total RNA was prepared from plants harvested at 0, 6, 12, 24, and 48 h for subsequent RNA sequencing. In total, 61,100 transcripts and 5,118 differentially expressed genes (DEGs) displaying up- or down-regulation were identified in pairwise comparisons of WT and DR plants following drought conditions. Transcriptome profiling showed the number of DEGs with up-regulation and down-regulation at 909, 977, 1181, 1225 and 826 between WT and DR plants at 0, 6, 12, 24, and 48 h, respectively. Results of KEGG enrichment showed that the drought tolerance mechanism of the DR plant can mainly be explained by two aspects, the 'photosynthetic-antenna protein' and 'protein processing of the endoplasmic reticulum'. We also divided eight expression patterns in four pairwise comparisons of DR plants (DR0 vs DR6, DR12, DR24, DR48) under PEG treatment. Our comprehensive transcriptome data will further enhance our understanding of the mechanisms regulating drought tolerance in tetraploid potato cultivars.

Keywords

References

  1. Andrews, S. (2010). FastQC: a quality control tool for high throughput sequence data.
  2. Anithakumari, A., Nataraja, K.N., Visser, R.G., and van der Linden, C.G. (2012). Genetic dissection of drought tolerance and recovery potential by quantitative trait locus mapping of a diploid potato population. Mol. Breeding 30, 1413-1429. https://doi.org/10.1007/s11032-012-9728-5
  3. Behera, M., Panigrahi, J., Mishra, R.R., and Rath, S.P. (2012). Analysis of EMS induced in vitro mutants of Asteracantha longifolia (L.) Nees using RAPD markers. Indian J. Biotechnol. 11, 39-47
  4. Bray, E.A. (2004). Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J. Exp. Bot. 55, 2331-2341. https://doi.org/10.1093/jxb/erh270
  5. Bray, N.L., Pimentel, H., Melsted, P., and Pachter, L. (2016). Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525. https://doi.org/10.1038/nbt.3519
  6. Cai, X., Davis, E.J., Ballif, J., Liang, M., Bushman, E., Haroldsen, V., Torabinejad, J., and Wu, Y. (2006). Mutant identification and characterization of the laccase gene family in Arabidopsis. J. Exp. Botany 57, 2563-2569. https://doi.org/10.1093/jxb/erl022
  7. Cartagena, J.A., Seki, M., Tanaka, M., Yamauchi, T., Sato, S., Hirakawa, H., and Tsuge, T. (2014). Gene expression profiles in jatropha under drought stress and during recovery. Plant Mol. Bio. Rep., 1-13.
  8. Chaves, M. (1991). Effects of water deficits on carbon assimilation. J. Exp. Botany 42, 1-16. https://doi.org/10.1093/jxb/42.1.1
  9. Chaves, M.M., Flexas, J., and Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 103, 551-560. https://doi.org/10.1093/aob/mcn125
  10. Chepyshko, H., Lai, C.-P., Huang, L.-M., Liu, J.-H., and Shaw, J.-F. (2012). Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: new insights from bioinformatics analysis. BMC Genomics 13, 309. https://doi.org/10.1186/1471-2164-13-309
  11. Cho, H.Y., Lee, C., Hwang, S.-G., Park, Y.C., Lim, H.L., and Jang, C.S. (2014). Overexpression of the OsChI1 gene, encoding a putative laccase precursor, increases tolerance to drought and salinity stress in transgenic Arabidopsis. Gene 552, 98-105. https://doi.org/10.1016/j.gene.2014.09.018
  12. Cloonan, N., Forrest, A.R., Kolle, G., Gardiner, B.B., Faulkner, G.J., Brown, M.K., Taylor, D.F., Steptoe, A.L., Wani, S., and Bethel, G. (2008). Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat. Methods 5, 613-619. https://doi.org/10.1038/nmeth.1223
  13. Dalla Costa, L., Delle Vedove, G., Gianquinto, G., Giovanardi, R., and Peressotti, A. (1997). Yield, water use efficiency and nitrogen uptake in potato: influence of drought stress. Potato Res. 40, 19-34. https://doi.org/10.1007/BF02407559
  14. Fischer, L., Lipavska, H., Hausman, J.-F., and Opatrny, Z. (2008). Morphological and molecular characterization of a spontaneously tuberizing potato mutant: an insight into the regulatory mechanisms of tuber induction. BMC Plant Biol. 8, 117. https://doi.org/10.1186/1471-2229-8-117
  15. Galvez, J.H., Tai, H.H., Lague, M., Zebarth, B.J., and Stromvik, M.V. (2016). The nitrogen responsive transcriptome in potato (Solanum tuberosum L.) reveals significant gene regulatory motifs. Sci. Rep. 6, 26090. https://doi.org/10.1038/srep26090
  16. Garg, R., Patel, R.K., Tyagi, A.K., and Jain, M. (2011). De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res. 18, 53-63. https://doi.org/10.1093/dnares/dsq028
  17. Gong, L., Zhang, H., Gan, X., Zhang, L., Chen, Y., Nie, F., Shi, L., Li, M., Guo, Z., and Zhang, G. (2015). Transcriptome Profiling of the Potato (Solanum tuberosum L.) Plant under Drought Stress and Water-Stimulus Conditions. PloS One 10, e0128041. https://doi.org/10.1371/journal.pone.0128041
  18. Haas, B.J., and Zody, M.C. (2010). Advancing RNA-seq analysis. Nat. Biotechnol. 28, 421-423. https://doi.org/10.1038/nbt0510-421
  19. Hirsch, C.D., Hamilton, J.P., Childs, K.L., Cepela, J., Crisovan, E., Vaillancourt, B., Hirsch, C.N., Habermann, M., Neal, B., and Buell, C.R. (2014). Spud DB: A resource for mining sequences, genotypes, and phenotypes to accelerate potato breeding. The Plant Genome 7.
  20. Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2008). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
  21. Hwang, S.-G., Kim, D.S., Hwang, J.E., Park, H.M., and Jang, C.S. (2015). Identification of altered metabolic pathways of $\gamma$-irradiated rice mutant via network-based transcriptome analysis. Genetica 143, 635-644. https://doi.org/10.1007/s10709-015-9861-2
  22. Iovieno, P., Punzo, P., Guida, G., Mistretta, C., Van Oosten, M.J., Nurcato, R., Bostan, H., Colantuono, C., Costa, A., and Bagnaresi, P. (2016). Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front. Plant Sci. 7, 371.
  23. Jabeen, N., and Mirza, B. (2004). Ethyl methane sulfonate induces morphological mutations in Capsicum annuum. Int. J. Agric. Biol. 6, 340-345.
  24. Jiang, H., Lei, R., Ding, S.-W., and Zhu, S. (2014). Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15, 182. https://doi.org/10.1186/1471-2105-15-182
  25. Jung, W.Y., Lee, S.S., Kim, C.W., Kim, H.-S., Min, S.R., Moon, J.S., Kwon, S.-Y., Jeon, J.-H., and Cho, H.S. (2014). RNA-Seq analysis and de novo transcriptome assembly of jerusalem artichoke (Helianthus tuberosus linne). PLoS One 9, e111982. https://doi.org/10.1371/journal.pone.0111982
  26. Khayatnezhad, M., and Gholamin, R. (2012). The effect of drought stress on leaf chlorophyll content and stress resistance in maize cultivars (Zea mays). Afr. J. Microbiol. Res. 6, 2844-2848.
  27. Kikuchi, A., Huynh, H.D., Endo, T., and Watanabe, K. (2015). Review of recent transgenic studies on abiotic stress tolerance and future molecular breeding in potato. Breeding Sci. 65, 85. https://doi.org/10.1270/jsbbs.65.85
  28. Kim, H.A., Shin, A.Y., Lee, M.S., Lee, H.J., Lee, H.R., Ahn, J., Nahm, S., Jo, S.H., Park, J.M., and Kwon, S.Y. (2016). De novo transcriptome analysis of Cucumis melo L. var. makuwa. Mol. Cells 39, 141. https://doi.org/10.14348/molcells.2016.2264
  29. Lane, B., Bernier, F., Dratewka-Kos, E., Shafai, R., Kennedy, T., Pyne, C., Munro, J., Vaughan, T., Walters, D., and Altomare, F. (1991). Homologies between members of the germin gene family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J. Biol. Chem. 266, 10461-10469.
  30. Lane, B., Dunwell, J.M., Ray, J., Schmitt, M., and Cuming, A. (1993). Germin, a protein marker of early plant development, is an oxalate oxidase. J. Biol. Chem. 268, 12239-12242.
  31. Li, B., and Dewey, C.N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323. https://doi.org/10.1186/1471-2105-12-323
  32. Li, H., Yao, W., Fu, Y., Li, S., and Guo, Q. (2015). De novo assembly and discovery of genes that are involved in drought tolerance in Tibetan Sophora moorcroftiana. PloS One 10, e111054. https://doi.org/10.1371/journal.pone.0111054
  33. Li, X., Zhang, Y., Yin, L., and Lu, J. (2017). Overexpression of pathogen-induced grapevine TIR-NB-LRR gene VaRGA1 enhances disease resistance and drought and salt tolerance in nicotiana benthamiana. Protoplasma 254, 957-969. https://doi.org/10.1007/s00709-016-1005-8
  34. Liu, H., Ma, Y., Chen, N., Guo, S., Liu, H., Guo, X., Chong, K., and Xu, Y. (2014). Overexpression of stress‐inducible OsBURP16, the $\beta$ subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice. Plant Cell Environ. 37, 1144-1158. https://doi.org/10.1111/pce.12223
  35. Liu, M., Shi, J., and Lu, C. (2013a). Identification of stress-responsive genes in Ammopiptanthus mongolicus using ESTs generated from cold-and drought-stressed seedlings. BMC Plant Biol. 13, 88. https://doi.org/10.1186/1471-2229-13-88
  36. Liu, T., Zhu, S., Tang, Q., Yu, Y., and Tang, S. (2013b). Identification of drought stress-responsive transcription factors in ramie (Boehmeria nivea L. gaud). BMC Plant Biology 13, 130. https://doi.org/10.1186/1471-2229-13-130
  37. Livaja, M., Wang, Y., Wieckhorst, S., Haseneyer, G., Seidel, M., Hahn, V., Knapp, S.J., Taudien, S., Schon, C.C., and Bauer, E. (2013). BSTA: a targeted approach combines bulked segregant analysis with next-generation sequencing and de novo transcriptome assembly for SNP discovery in sunflower. BMC Genomics 14, 628. https://doi.org/10.1186/1471-2164-14-628
  38. Luan, Y.S., Zhang, J., Gao, X.R., and An, L.J. (2007). Mutation induced by ethylmethanesulphonate (EMS), in vitro screening for salt tolerance and plant regeneration of sweet potato (Ipomoea batatas L.). Plant Cell Tiss. Organ. Cult. 88, 77-81. https://doi.org/10.1007/s11240-006-9183-2
  39. Massa, A.N., Childs, K.L., and Buell, C.R. (2013). Abiotic and biotic stress responses in Solanum tuberosum group Phureja DM1-3 516 R44 as measured through whole transcriptome sequencing. The Plant Genome 6.
  40. Massa, A.N., Childs, K.L., Lin, H., Bryan, G.J., Giuliano, G., and Buell, C.R. (2011). The transcriptome of the reference potato genome Solanum tuberosum Group Phureja clone DM1-3 516R44. Plos One 6, e26801. https://doi.org/10.1371/journal.pone.0026801
  41. Mizuno, H., Kawahigashi, H., Kawahara, Y., Kanamori, H., Ogata, J., Minami, H., Itoh, T., and Matsumoto, T. (2012). Global transcriptome analysis reveals distinct expression among duplicated genes during sorghum-Bipolaris sorghicola interaction. BMC Plant Biol. 12, 121. https://doi.org/10.1186/1471-2229-12-121
  42. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A.C., and Kanehisa, M. (2007). KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, W182-W185. https://doi.org/10.1093/nar/gkm321
  43. Mudalkar, S., Golla, R., Ghatty, S., and Reddy, A.R. (2014). De novo transcriptome analysis of an imminent biofuel crop, Camelina sativa L. using Illumina GAIIX sequencing platform and identification of SSR markers. Plant Mol. Biol. 84, 159-171. https://doi.org/10.1007/s11103-013-0125-1
  44. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plantarum 15, 473-497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
  45. Muth, J., Hartje, S., Twyman, R.M., Hofferbert, H.R., Tacke, E., and Prufer, D. (2008). Precision breeding for novel starch variants in potato. Plant. Biotechnol. J. 6, 576-584. https://doi.org/10.1111/j.1467-7652.2008.00340.x
  46. Parry, M.A., Madgwick, P.J., Bayon, C., Tearall, K., Hernandez-Lopez, A., Baudo, M., Rakszegi, M., Hamada, W., Al-Yassin, A., and Ouabbou, H. (2009). Mutation discovery for crop improvement. J. Exp. Bot. 60, 2817-2825. https://doi.org/10.1093/jxb/erp189
  47. Pathirana, R. (2012). Plant mutation breeding in agriculture. Plant Sci. Rev. 2011, 107.
  48. Sampedro, J., and Cosgrove, D.J. (2005). The expansin superfamily. Genome Biology 6, 242. https://doi.org/10.1186/gb-2005-6-12-242
  49. Schulz, M.H., Zerbino, D.R., Vingron, M., and Birney, E. (2012). Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086-1092. https://doi.org/10.1093/bioinformatics/bts094
  50. Shu, Q., Forster, B., and Nakagawa, H. (2012). Principles and applications of plant mutation breeding. Plant Mutation Breeding and Biotechnology, 301-325.
  51. Sikora, P., Chawade, A., Larsson, M., Olsson, J., and Olsson, O. (2011). Mutagenesis as a tool in plant genetics, functional genomics, and breeding. Int. J. Plant Genomics 2011.
  52. Sivamani, E., Bahieldin, A., Wraith, J.M., Al-Niemi, T., Dyer, W.E., Ho, T.-H.D., and Qu, R. (2000). Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci. 155, 1-9. https://doi.org/10.1016/S0168-9452(99)00247-2
  53. Taheri, S., Abdullah, T.L., Jain, S.M., Sahebi, M., and Azizi, P. (2017). TILLING, high-resolution melting (HRM), and next-generation sequencing (NGS) techniques in plant mutation breeding. Mol. Breeding 37, 40. https://doi.org/10.1007/s11032-017-0643-7
  54. Tan, Y., Li, M., Yang, Y., Sun, X., Wang, N., Liang, B., and Ma, F. (2017). Overexpression of MpCYS4, a phytocystatin gene from Malus prunifolia (Willd.) Borkh., enhances stomatal closure to confer drought tolerance in transgenic Arabidopsis and apple. Front. Plant Sci. 8, 33.
  55. Tarazona, S., Furio-Tari, P., Turra, D., Pietro, A.D., Nueda, M.J., Ferrer, A., and Conesa, A. (2015). Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package. Nucleic Acids Res. 43, e140-e140.
  56. Thimm, O., Blaesing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., and Stitt, M. (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939. https://doi.org/10.1111/j.1365-313X.2004.02016.x
  57. Uitdewilligen, J.G., Wolters, A.-M.A., Bjorn, B., Borm, T.J., Visser, R.G., and van Eck, H.J. (2013). A next-generation sequencing method for genotyping-by-sequencing of highly heterozygous autotetraploid potato. PLoS One 8, e62355. https://doi.org/10.1371/journal.pone.0062355
  58. Vera, J.C., Wheat, C.W., Fescemyer, H.W., Frilander, M.J., Crawford, D.L., Hanski, I., and Marden, J.H. (2008). Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol. Ecol. 17, 1636-1647. https://doi.org/10.1111/j.1365-294X.2008.03666.x
  59. Vos, J., and Groenwold, J. (1986). Root growth of potato crops on a marine-clay soil. Plant Soil 94, 17-33. https://doi.org/10.1007/BF02380587
  60. Wang, Z., Gerstein, M., and Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63. https://doi.org/10.1038/nrg2484
  61. Xu, X., Pan, S., Cheng, S., Zhang, B., Bachem, C., de Boer, J., Borm, T., Kloosterman, B., van Eck, H., and Datema, E. (2011). Genome sequence and analysis of the tuber crop potato. Nature 475, 189-195. https://doi.org/10.1038/nature10158
  62. Xu, Y., Gao, S., Yang, Y., Huang, M., Cheng, L., Wei, Q., Fei, Z., Gao, J., and Hong, B. (2013). Transcriptome sequencing and whole genome expression profiling of chrysanthemum under dehydration stress. BMC Genomics 14, 662. https://doi.org/10.1186/1471-2164-14-662
  63. Yates, S.A., Swain, M.T., Hegarty, M.J., Chernukin, I., Lowe, M., Allison, G.G., Ruttink, T., Abberton, M.T., Jenkins, G., and Skot, L. (2014). De novo assembly of red clover transcriptome based on RNA-Seq data provides insight into drought response, gene discovery and marker identification. BMC Genomics 15, 453. https://doi.org/10.1186/1471-2164-15-453
  64. Yaycili, O., and Alikamanoglu, S. (2012). Induction of salt-tolerant potato (Solanum tuberosum L.) mutants with gamma irradiation and characterization of genetic variations via RAPD-PCR analysis. Turk J. Biol. 36, 405-412.
  65. Zerbino, D.R., and Birney, E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829. https://doi.org/10.1101/gr.074492.107
  66. Zhang, N., Liu, B., Ma, C., Zhang, G., Chang, J., Si, H., and Wang, D. (2014). Transcriptome characterization and sequencing-based identification of drought-responsive genes in potato. Mol. Biol. Rep. 41, 505-517. https://doi.org/10.1007/s11033-013-2886-7
  67. Zhang, X., Liu, S., and Takano, T. (2008). Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol. Biol. 68, 131-143. https://doi.org/10.1007/s11103-008-9357-x
  68. Zhao, M.R., Han, Y.Y., Feng, Y.N., Li, F., and Wang, W. (2012). Expansins are involved in cell growth mediated by abscisic acid and indole-3-acetic acid under drought stress in wheat. Plant Cell Rep. 31, 671-685. https://doi.org/10.1007/s00299-011-1185-9

Cited by

  1. Comparative Transcriptomic Analysis of MAPK-Mediated Regulation of Sectorization in Cryphonectria parasitica vol.42, pp.4, 2018, https://doi.org/10.14348/molcells.2019.0019
  2. Molecular characterization of Helianthus tuberosus L. treated with ethyl methanesulfonate based on inter-simple sequence repeat markers vol.16, pp.9, 2018, https://doi.org/10.1007/s13762-019-02486-1
  3. Structural genome analysis in cultivated potato taxa vol.133, pp.3, 2018, https://doi.org/10.1007/s00122-019-03519-6
  4. Comparative physiological and proteomic analysis indicates lower shock response to drought stress conditions in a self-pollinating perennial ryegrass vol.15, pp.6, 2018, https://doi.org/10.1371/journal.pone.0234317
  5. A Novel Banana Mutant “RF 1” (Musa spp. ABB, Pisang Awak Subgroup) for Improved Agronomic Traits and Enhanced Cold Tolerance and Disease Resistance vol.12, pp.None, 2018, https://doi.org/10.3389/fpls.2021.730718
  6. Genome-Wide Approach to Identify Quantitative Trait Loci for Drought Tolerance in Tetraploid Potato (Solanum tuberosum L.) vol.22, pp.11, 2018, https://doi.org/10.3390/ijms22116123
  7. De novo Transcriptome Assembly and Comprehensive Annotation of Two Tree Tomato Cultivars (Solanum betaceum Cav.) with Different Fruit Color vol.7, pp.11, 2021, https://doi.org/10.3390/horticulturae7110431
  8. Improving the Tea Withering Process Using Ethylene or UV-C vol.69, pp.45, 2018, https://doi.org/10.1021/acs.jafc.1c02876
  9. Transcriptome analysis of Kentucky bluegrass subject to drought and ethephon treatment vol.16, pp.12, 2018, https://doi.org/10.1371/journal.pone.0261472