Journal of Ginseng Research

  • 제48권5호
  • /
  • Pages.511-519
  • /
  • 2024
  • /
  • 1226-8453(pISSN)
  • /
  • 2093-4947(eISSN)
고려인삼학회 (The Korean Society of Ginseng)
권호 표지
DOI QR코드

DOI QR Code

Identification of a key signaling network regulating perennating bud dormancy in Panax ginseng

  • Jeoungeui Hong (Department of Biology, Chungbuk National University) ;
  • Soeun Han (Department of Biology, Chungbuk National University) ;
  • Kyoung Rok Geem (Department of Biology, Chungbuk National University) ;
  • Wonsil Bae (Department of Biology, Chungbuk National University) ;
  • Jiyong Kim (School of Biological Sciences, Seoul National University) ;
  • Moo-Geun Jee (Ginseng & Medicinal Plant Research Institute, Chungnam Agricultural Research & Extension Service) ;
  • Jung-Woo Lee (Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Jang-Uk Kim (Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Gisuk Lee (Department of Biological Sciences, Korea Advanced Institute for Science and Technology) ;
  • Youngsung Joo (School of Biological Sciences, Seoul National University) ;
  • Donghwan Shim (Department of Biological Sciences, Chungnam National University) ;
  • Hojin Ryu (Department of Biology, Chungbuk National University)
  • 투고 : 2024.02.14
  • 심사 : 2024.04.19
  • 발행 : 2024.09.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Background: The cycle of seasonal dormancy of perennating buds is an essential adaptation of perennial plants to unfavorable winter conditions. Plant hormones are key regulators of this critical biological process, which is intricately connected with diverse internal and external factors. Recently, global warming has increased the frequency of aberrant temperature events that negatively affect the dormancy cycle of perennials. Although many studies have been conducted on the perennating organs of Panax ginseng, the molecular aspects of bud dormancy in this species remain largely unknown. Methods: In this study, the molecular physiological responses of three P. ginseng cultivars with different dormancy break phenotypes in the spring were dissected using comparative genome-wide RNA-seq and network analyses. These analyses identified a key role for abscisic acid (ABA) activity in the regulation of bud dormancy. Gene set enrichment analysis revealed that a transcriptional network comprising stress-related hormone responses made a major contribution to the maintenance of dormancy. Results: Increased expression levels of cold response and photosynthesis-related genes were associated with the transition from dormancy to active growth in perennating buds. Finally, the expression patterns of genes encoding ABA transporters, receptors (PYRs/PYLs), PROTEIN PHOSPHATASE 2Cs (PP2Cs), and DELLAs were highly correlated with different dormancy states in three P. ginseng cultivars. Conclusion: This study provides evidence that ABA and stress signaling outputs are intricately connected with a key signaling network to regulate bud dormancy under seasonal conditions in the perennial plant P. ginseng.

키워드

과제정보

This work was supported by the Cooperative Research Program for Agriculture Science & Technology Development (No. PJ01482004).

참고문헌

  1. Ahuja A, Kim JH, Kim J-H, Yi Y-S, Cho JY. Functional role of ginseng-derived compounds in cancer. Journal of ginseng research 2018;42:248-54. 
  2. Arring NM, Millstine D, Marks LA, Nail LM. Ginseng as a treatment for fatigue: a systematic review. J Alternative Compl Med 2018;24:624-33. 
  3. Choi Kt. Botanical characteristics, pharmacological effects and medicinal components of Korean Panax ginseng CA Meyer. Acta Pharmacol Sin 2008;29:1109-18. 
  4. Kim Y-S, Park C-S, Lee D-Y, Lee J-S, Lee S-H, In J-G, Hong T-K. Phenological growth stages of Korean ginseng (Panax ginseng) according to the extended BBCH scale. Journal of Ginseng Research 2021;45:527-34. 
  5. Chen T, Wang L, Wang H, Jiang S, Zhou S. Photoperiod and temperature as dominant environmental drivers triggering plant phenological development of American ginseng along with its quality formation. Front Earth Sci 2022;10:894251. 
  6. Hong J, Geem KR, Kim J, Jo I-H, Yang T-J, Shim D, Ryu H. Prolonged exposure to high temperature inhibits shoot primary and root secondary growth in Panax ginseng. Int J Mol Sci 2022;23:11647. 
  7. Lee J-S, Lee J-H, Ahn I-O. Characteristics of resistant lines to high-temperature injury in ginseng (Panax ginseng CA Meyer). Journal of Ginseng Research 2010;34:274-81. 
  8. Lee K-M, Kim H-R, Lim H, You Y-H. Effect of elevated CO 2 concentration and temperature on the growth and ecophysiological responses of ginseng (Panax ginseng CA Meyer). Korean Journal of Crop Science 2012;57:106-12. 
  9. Suh S, Moon J, Kwon N, Jang I, Kim Y, Jang I. Effects of cold temperature and relative humidity on the freezing stress of two year-old ginseng seedlings. Korean Journal of Medicinal Crop Science. 2021;29:194-200. 
  10. Suh S, Yu J, Kim D, Jang I. Influence of freezing damage during sprouting periods on root growth characteristics and saponin contents in Panax ginseng C. A. Meyer. Korean Journal of Medicinal Crop Science. 2022;30:99-107. 
  11. Shuai H, Meng Y, Luo X, Chen F, Zhou W, Dai Y, et al. Exogenous auxin represses soybean seed germination through decreasing the gibberellin/abscisic acid (GA/ABA) ratio. Sci Rep 2017;7:12620. 
  12. Shu K, Zhou W, Chen F, Luo X, Yang W. Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 2018;9:416. 
  13. Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A, Singh RK, et al. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science 2018;360:212-5. 
  14. Bao S, Hua C, Shen L, Yu H. New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 2020;62:118-31. 
  15. Nagai K, Mori Y, Ishikawa S, Furuta T, Gamuyao R, Niimi Y, et al. Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature 2020;584:109-14. 
  16. Kim YC, Kim YB, Park HW, Bang KH, Kim JU, Jo IH, et al. Optimal harvesting time of ginseng seeds and effect of gibberellic acid (GA 3) treatment for improving stratification rate of ginseng (Panax ginseng CA Meyer) seeds. Korean Journal of Medicinal Crop Science. 2014;22:423-8. 
  17. Hong CP, Jang GY, Ryu H. Gibberellins enhance plant growth and ginsenoside content in Panax ginseng. J Plant Biotechnol 2021;48:186-92. 
  18. Hong CP, Kim J, Lee J, Yoo S-i, Bae W, Geem KR, et al. Gibberellin signaling promotes the secondary growth of storage roots in Panax ginseng. Int J Mol Sci 2021;22:8694. 
  19. Ge N, Jia J-S, Yang L, Huang R-M, Wang Q-Y, Chen C, et al. Exogenous gibberellic acid shortening after-ripening process and promoting seed germination in a medicinal plant Panax notoginseng. BMC Plant Biol 2023;23:67. 
  20. Kim J, Shin W-R, Kim Y-H, Shim D, Ryu H. Functional characterization of gibberellin signaling-related genes in Panax ginseng. J Plant Biotechnol 2021;48:148-55. 
  21. Rolston L, Proctor J, Fletcher R, Murr D. Gibberellin effects on inflorescence development, bud dormancy and root development in North American Ginseng. Journal of Ginseng Research 2002;26:17-23. 
  22. Kim DH, Kim YC, Bang KH, Kim JU, Lee JW, Cho IH, et al. Effects of GA 3 and alternating temperature on breaking bud dormancy of Panax ginseng CA Meyer Seedling. Korean Journal of Medicinal Crop Science. 2015;23:379-84. 
  23. Castro-Camba R, S' anchez C, Vidal N, Vielba JM. Interactions of gibberellins with phytohormones and their role in stress responses. Horticulturae 2022;8:241. 
  24. Liu J, Sherif SM. Hormonal orchestration of bud dormancy cycle in deciduous woody perennials. Front Plant Sci 2019;10:1136. 
  25. Ophir R, Pang X, Halaly T, Venkateswari J, Lavee S, Galbraith D, Or E. Gene-expression profiling of grape bud response to two alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement. Plant Mol Biol 2009;71:403. 
  26. Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E. Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 2015;66:1527-42. 
  27. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011;27:863-4. 
  28. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357-9. 
  29. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 2011;12:1-16. 
  30. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139-40. 
  31. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 2013;8:1494-512. 
  32. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009;37:1-13. 
  33. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57. 
  34. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles, vol. 102. Proceedings of the National Academy of Sciences; 2005. p. 15545-50. 
  35. Montojo J, Zuberi K, Rodriguez H, Kazi F, Wright G, Donaldson SL, et al. GeneMANIA Cytoscape plugin: fast gene function predictions on the desktop. Bioinformatics 2010;26:2927-8. 
  36. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003;13:2498-504. 
  37. Joo Y, Kim H, Kang M, Lee G, Choung S, Kaur H, et al. Pith-specific lignification in Nicotiana attenuata as a defense against a stem-boring herbivore. New Phytol 2021;232:332-44. 
  38. Schafer M, Brutting C, Baldwin IT, Kallenbach M. High-throughput quantification of more than 100 primary-and secondary-metabolites, and phytohormones by a single solid-phase extraction based sample preparation with analysis by UHPLC-HESI-MS/MS. Plant Methods 2016;12:1-18. 
  39. Park HJ, Nam BE, Lee G, Kim S-G, Joo Y, Kim JG. Ontogeny-dependent effects of elevated CO2 and watering frequency on interaction between Aristolochia contorta and its herbivores. Sci Total Environ 2022;838:156065. 
  40. Bang K-H, Kim Y-C, Lee J-W, Cho I-H, Hong C-E, Hyun D-Y, Kim J-U. Major achievement and prospect of ginseng breeding in Korea. Korean Society of Breeding Science 2020;52:170-8. 
  41. Bhaskara GB, Nguyen TT, Verslues PE. Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol 2012;160:379-95. 
  42. Chen C-C, Liang C-S, Kao A-L, Yang C-C. HHP1, a novel signalling component in the cross-talk between the cold and osmotic signalling pathways in Arabidopsis. J Exp Bot 2010;61:3305-20. 
  43. Li Y, Zhang L, Li D, Liu Z, Wang J, Li X, Yang Y. The Arabidopsis F-box E3 ligase RIFP1 plays a negative role in abscisic acid signalling by facilitating ABA receptor RCAR3 degradation. Plant Cell Environ 2016;39:571-82. 
  44. Hong J, Kim H, Ryu H. Identification of ABSCISIC ACID (ABA) signaling related genes in Panax ginseng. J Plant Biotechnol 2018;45:306-14. 
  45. Kang J, Yim S, Choi H, Kim A, Lee KP, Lopez-Molina L, et al. Abscisic acid transporters cooperate to control seed germination. Nat Commun 2015;6:8113. 
  46. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, et al. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor, vol. 109. Proceedings of the National Academy of Sciences; 2012. p. 9653-8. 
  47. Carrillo-Barral N, Rodriguez-Gacio MdC, Matilla A. Delay of Germination-1 (DOG1): a key to understanding seed dormancy. Plants 2020;9:480. 
  48. Nishimura N, Tsuchiya W, Moresco JJ, Hayashi Y, Satoh K, Kaiwa N, et al. Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nat Commun 2018;9:1-14. 
  49. Mohanty B. Genomic architecture of promoters and transcriptional regulation of candidate genes in rice involved in tolerance to anaerobic germination. Current Plant Biology 2022;29:100236. 
  50. Parmesan C, Morecroft MD, Trisurat Y. Climate change 2022: impacts, adaptation and vulnerability: giec. 2022. 
  51. Horvath DP, Anderson JV, Chao WS, Foley ME. Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 2003;8:534-40. 
  52. Rohde A, Boerjan W. Insights into bud development and dormancy in poplar. Trends in European Forest Tree Physiology Research: Cost Action E6: EUROSILVA. 2001:33-52. 
  53. Yamane H. Regulation of bud dormancy and bud break in Japanese apricot (Prunus mume Siebold & Zucc.) and peach [Prunus persica (L.) Batsch]: a summary of recent studies. J Jpn Soc Hortic Sci 2014;83:187-202. 
  54. Chung C, Ahn S, Kwon W. Effects of the growth regulators on the emergence and growth of Panax ginseng CA Meyer. Korean Journal of Crop Science 1985;30: 368-74. 
  55. Pan W, Liang J, Sui J, Li J, Liu C, Xin Y, et al. ABA and bud dormancy in perennials: current knowledge and future perspective. Genes 2021;12:1635. 
  56. Zhang Z, Zhuo X, Zhao K, Zheng T, Han Y, Yuan C, Zhang Q. Transcriptome profiles reveal the crucial roles of hormone and sugar in the bud dormancy of Prunus mume. Sci Rep 2018;8:5090. 
  57. Chengguo D, Xianli L, Dongsheng G, Huanfang L, Meng L. Studies on regulations of endogenous ABA and GA3 in sweet cherry FlowerBuds on dormancy. Acta Hortic Sin 2004;31:149. 
  58. Orrantia-Araujo MA, Martinez-T'ellez MA, ' Rivera-Dominguez M, Hern' andezOnate ˜ MA, ' Vargas-Arispuro I. Changes in the endogenous content and gene expression of salicylic acid correlate with grapevine bud dormancy release. J Plant Growth Regul 2021;40:254-62. 
  59. Casazza AP, Rossini S, Rosso MG, Soave C. Mutational and expression analysis of ELIP1 and ELIP2 in Arabidopsis thaliana. Plant Mol Biol 2005;58:41-51. 
  60. Gould PD, Locke JC, Larue C, Southern MM, Davis SJ, Hanano S, et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 2006;18:1177-87. 
  61. Hong J, Ryu H. Identification and functional analysis of COLD-signaling-related genes in Panax ginseng. J Plant Biotechnol 2023;50:225-31. 
  62. Kidokoro S, Hayashi K, Haraguchi H, Ishikawa T, Soma F, Konoura I, et al. Posttranslational regulation of multiple clock-related transcription factors triggers cold-inducible gene expression in Arabidopsis, vol. 118. Proceedings of the National Academy of Sciences; 2021, e2021048118. 
  63. Kim D-H, Sung S. Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 2013;25:454-69.