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Comparative transcriptome analysis of heat stress responsiveness between two contrasting ginseng cultivars

  • Jayakodi, Murukarthick (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Lee, Sang-Choon (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Yang, Tae-Jin (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University)
  • Received : 2017.10.28
  • Accepted : 2018.05.28
  • Published : 2019.10.15

Abstract

Background: Panax ginseng has been used in traditional medicine to strengthen the body and mental well-being of humans for thousands of years. Many elite ginseng cultivars have been developed, and ginseng cultivation has become well established during the last century. However, heat stress poses an important threat to the growth and sustainable production of ginseng. Efforts have been made to study the effects of high temperature on ginseng physiology, but knowledge of the molecular responses to heat stress is still limited. Methods: We sequenced the transcriptomes (RNA-Seq) of two ginseng cultivars, Chunpoong (CP) and Yunpoong (YP), which are sensitive and resistant to heat stress, respectively, after 1- and 3-week heat treatments. Differential gene expression and gene ontology enrichment along with profiled chlorophyll contents were performed. Results: CP is more sensitive to heat stress than YP and exhibited a lower chlorophyll content than YP. Moreover, heat stress reduced the chlorophyll content more rapidly in CP than in YP. A total of 329 heat-responsive genes were identified. Intriguingly, genes encoding chlorophyll a/b-binding proteins, WRKY transcription factors, and fatty acid desaturase were predominantly responsive during heat stress and appeared to regulate photosynthesis. In addition, a genome-wide scan of photosynthetic and sugar metabolic genes revealed reduced transcription levels for ribulose 1,5-bisphosphate carboxylase/oxygenase under heat stress, especially in CP, possibly attributable to elevated levels of soluble sugars. Conclusion: Our comprehensive genomic analysis reveals candidate loci/gene targets for breeding and functional studies related to developing high temperature-tolerant ginseng varieties.

Keywords

References

  1. Ahuja I, de Vos RC, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci 2010;15(12):664-74. https://doi.org/10.1016/j.tplants.2010.08.002
  2. Krasensky J, Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 2012;63(4):1593-608. https://doi.org/10.1093/jxb/err460
  3. Boyer JS. Plant productivity and environment. Science 1982;218(4571):443-8. https://doi.org/10.1126/science.218.4571.443
  4. Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci 2006;11(1):15-9. https://doi.org/10.1016/j.tplants.2005.11.002
  5. Change IPoC. Climate change 2014-impacts, adaptation and vulnerability: regional aspects. Cambridge University Press; 2014.
  6. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD. Complexity of the heat stress response in plants. Curr Opin Plant Biol 2007;10(3):310-6. https://doi.org/10.1016/j.pbi.2007.04.011
  7. Qu AL, Ding YF, Jiang Q, Zhu C. Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 2013;432(2):203-7. https://doi.org/10.1016/j.bbrc.2013.01.104
  8. Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 2013;4:273. https://doi.org/10.3389/fpls.2013.00273
  9. Ortiz R, Braun HJ, Crossa J, Crouch JH, Davenport G, Dixon J, Dreisigacker S, Duveiller E, He Z, Huerta J, et al. Wheat genetic resources enhancement by the International Maize and Wheat Improvement Center (CIMMYT). Genet Resour Crop Evol 2008;55(7):1095-140. https://doi.org/10.1007/s10722-008-9372-4
  10. Lipiec J, Doussan C, Nosalewicz A, Kondracka K. Effect of drought and heat stresses on plant growth and yield: a review. Int. Agrophys 2013;27(4):463-77. https://doi.org/10.2478/intag-2013-0017
  11. Kim YJ, Zhang D, Yang DC. Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 2015;33(6):717-35. https://doi.org/10.1016/j.biotechadv.2015.03.001
  12. WE C. Ginseng: the genus Panax. UK: Taylor & Francis e-Library; 2006.
  13. Baeg IH, So SH. The world ginseng market and the ginseng (Korea). J Ginseng Res 2013;37(1):1-7. https://doi.org/10.5142/jgr.2013.37.1
  14. Lee JS, Lee DY, Lee JH, Ahn IO, In JG. Photosynthetic characteristics of resistance and susceptible lines to high temperature injury in Panax ginseng Meyer. J Ginseng Res 2012;36:461-8. https://doi.org/10.5142/jgr.2012.36.4.461
  15. Lee JS, Lee KH, Lee SS, Kim ES, Ahn IO, In JG. Morphological characteristics of ginseng leaves in high-temperature injury resistant and susceptible lines of Panax ginseng Meyer. J Ginseng Res 2011;35(4):449-56. https://doi.org/10.5142/jgr.2011.35.4.449
  16. Lee JS, Lee JH, Ahn IO. Characteristics of resistant lines to high-temperature injury in ginseng (Panax ginseng CA Meyer). J Ginseng Res 2010;34(4):274-81. https://doi.org/10.5142/jgr.2010.34.4.274
  17. Li H, Durbin R. Fast and accurate short read alignment with BurrowseWheeler transform. Bioinformatics 2009;25(14):1754-60. https://doi.org/10.1093/bioinformatics/btp324
  18. Xu H, Luo X, Qian J, Pang X, Song J, Qian G, Chen J, Chen S. FastUniq: a fast de novo duplicates removal tool for paired short reads. PLoS One 2012;7(12):e52249. https://doi.org/10.1371/journal.pone.0052249
  19. Kopylova E, Noe L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 2012;28(24):3211-7. https://doi.org/10.1093/bioinformatics/bts611
  20. Patel RK, Jain M. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PloS One 2012;7(2), e30619. https://doi.org/10.1371/journal.pone.0030619
  21. Jayakodi M, Choi BS, Lee SC, Kim NH, Park JY, Jang W, Lakshmanan M, Mohan SVG, Lee DY, Yang TJ. Ginseng Genome Database: an open-access platform for genomics of Panax ginseng. BMC Plant Biol 2018;18:62. https://doi.org/10.1186/s12870-018-1282-9
  22. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 2011;12:323. https://doi.org/10.1186/1471-2105-12-323
  23. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, Keime C, Marot G, Castel D, Estelle J, et al. A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform 2013;14(6):671-83. https://doi.org/10.1093/bib/bbs046
  24. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26(1):139-40. https://doi.org/10.1093/bioinformatics/btp616
  25. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014;30(9):1236-40. https://doi.org/10.1093/bioinformatics/btu031
  26. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007;35:182-5. https://doi.org/10.1093/nar/gkm321
  27. Mathur S, Agrawal D, Jajoo A. Photosynthesis: response to high temperature stress. J Photochem Photobiol B 2014;137:116-26. https://doi.org/10.1016/j.jphotobiol.2014.01.010
  28. Morales D, Rodriguez P, Dell'Amico J, Nicolas E, Torrecillas A, Sanchez-Blanco M. High-temperature preconditioning and thermal shock imposition affects water relations, gas exchange and root hydraulic conductivity in tomato. Biologia Plantarum 2003;47(2):203. https://doi.org/10.1023/B:BIOP.0000022252.70836.fc
  29. Bakshi M, Oelmuller R. WRKY transcription factors: jack of many trades in plants. Plant Signal Behav 2014;9(2), e27700. https://doi.org/10.4161/psb.27700
  30. Li S, Zhou X, Chen L, Huang W, Yu D. Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 2010;29(5):475-83. https://doi.org/10.1007/s10059-010-0059-2
  31. Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ, Wang X, Qiu AL, Zhang TX, Lin J, et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 2013;36(4):757-74. https://doi.org/10.1111/pce.12011
  32. Hazel JR, Williams EE. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 1990;29(3):167-227. https://doi.org/10.1016/0163-7827(90)90002-3
  33. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K. Trienoic fatty acids and plant tolerance of high temperature. Science 2000;287(5452):476-9. https://doi.org/10.1126/science.287.5452.476
  34. Sohn S, Back K. Transgenic rice tolerant to high temperature with elevated contents of dienoic fatty acids. Biologia Plantarum 2007;51(2):340-2. https://doi.org/10.1007/s10535-007-0067-z
  35. Wang HS, Yu C, Tang XF, Wang LY, Dong XC, Meng QW. Antisense-mediated depletion of tomato endoplasmic reticulum omega-3 fatty acid desaturase enhances thermal tolerance. J Integr Plant Biol 2010;52(6):568-77. https://doi.org/10.1111/j.1744-7909.2010.00957.x
  36. Upchurch RG. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 2008;30(6):967-77. https://doi.org/10.1007/s10529-008-9639-z
  37. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y. Genetically engineered alteration in the chilling sensitivity of plants. Nature 1992;356:710-3. https://doi.org/10.1038/356710a0
  38. Kim NH, Jayakodi M, Lee SC, Choi BS, Jang W, Lee J, Kim HH, Waminal NE, Lakshmanan M, van Nguyen B, et al. Genome and evolution of the shaderequiring medicinal herb Panax ginseng. Plant Biotechnol J 2018. https://doi.org/10.1111/pbi.12926.
  39. Jean-Marc R, Steven FF, John B. Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol 2000;124(4):1697-705. https://doi.org/10.1104/pp.124.4.1697
  40. Hormann F, Kuchler M, Sveshnikov D, Oppermann U, Li Y, Soll J. Tic32, an essential component in chloroplast biogenesis. J Biol Chem 2004;279(33):34756-62. https://doi.org/10.1074/jbc.M402817200
  41. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 2004;134(4):1683-96. https://doi.org/10.1104/pp.103.033431
  42. Jang JC, Leon P, Zhou L, Sheen J. Hexokinase as a sugar sensor in higher plants. Plant Cell 1997;9(1):5-19. https://doi.org/10.2307/3870367
  43. Miskell JH, Parmenter G, Eaton-Rye JJ. Photoperiodic changes of soluble sugar levels in Panax ginseng. Science Access 2001;3(1).
  44. Tholen D, Pons TL, Voesenek LA, Poorter H. Ethylene insensitivity results in down-regulation of rubisco expression and photosynthetic capacity in tobacco. Plant Physiol 2007;144(3):1305-15. https://doi.org/10.1104/pp.107.099762

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