Journal of Plant Biotechnology

  • Volume 50
  • /
  • Pages.225-231
  • /
  • 2023
  • /
  • 1229-2818(pISSN)
  • /
  • 2384-1397(eISSN)
The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Identification and functional analysis of COLD-signaling-related genes in Panax ginseng

  • Jeongeui Hong (Department of Biology, Chungbuk National University) ;
  • Hojin Ryu (Department of Biology, Chungbuk National University)
  • Received : 2023.11.05
  • Accepted : 2023.11.09
  • Published : 2023.11.21
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Abstract

Cold stress is one of the most vulnerable environmental stresses that affect plant growth and crop yields. With the recent advancements in genetic approaches using Arabidopsis and other model systems, genes involved in cold-stress response have been identified and the key cold signaling factors have been characterized. Exposure to low-temperature stress triggers the activation of a set of genes known as cold regulatory (COR) genes. This activation process plays a crucial role in enhancing the resistance of plants to cold and freezing stress. The inducer of the C-repeatbinding factor (CBF) expression 1-CBF module (ICE1-CBF module) is a key cold signaling pathway regulator that enhances the expression of downstream COR genes; however, this signaling module in Panax ginseng remains elusive. Here, we identified cold-signaling-related genes, PgCBF1, PgCBF3, and PgICE1 and conducted functional genomic analysis with a heterologous system. We confirmed that the overexpression of cold- PgCBF3 in the cbf1/2/3 triple Arabidopsis mutant compensated for the cold stress-induced deficiency of COR15A and salt-stress tolerance. In addition, nuclearlocalized PgICE1 has evolutionarily conserved phosphorylation sites that are modulated by brassinsteroid insensitive 2 (PgBIN2) and sucrose non-fermenting 1 (SNF1)-related protein kinase 3 (PgSnRK3), with which it physically interacted in a yeast two-hybrid assay. Overall, our data reveal that the regulators identified in our study, PgICE1 and PgCBFs, are evolutionarily conserved in the P. ginseng genome and are functionally involved in cold and abiotic stress responses.

Keywords

Acknowledgement

This research was supported by Chungbuk National University Korea National University Development Project (2023).

References

  1. Agarwal M, Hao Y, Kapoor A, Dong C-H, Fujii H, Zheng X, Zhu J-K (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. Journal of Biological Chemistry 281(49):37636-37645 https://doi.org/10.1074/jbc.M605895200
  2. Chinnusamy V, Ohta M, Kanrar S, Lee B-h, Hong X, Agarwal M, Zhu J-K (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes & development 17(8):1043-1054
  3. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Developmental cell 32(3):278-289 https://doi.org/10.1016/j.devcel.2014.12.023
  4. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in coldregulated gene expression and freezing tolerance. The Plant Cell 21(3):972-984
  5. Dong C-H, Agarwal M, Zhang Y, Xie Q, Zhu J-K (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proceedings of the National Academy of Sciences 103(21):8281-8286
  6. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant molecular biology 54:767-781 https://doi.org/10.1023/B:PLAN.0000040902.06881.d4
  7. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal 16(4):433-442
  8. Hong J, Kim H, Ryu H (2018) Identification of ABSCISIC ACID (ABA) signaling related genes in Panax ginseng. Journal of Plant Biotechnology 45(4):306-314 https://doi.org/10.5010/JPB.2018.45.4.306
  9. Hong J, Ryu H (2022) Identification of WAT1-like genes in Panax ginseng and functional analysis in secondary growth. Journal of Plant Biotechnology 49(3):171-177 https://doi.org/10.5010/JPB.2022.49.3.171
  10. Hwang H, Lee H-Y, Ryu H, Cho H (2020) Functional characterization of BRASSINAZOLE-RESISTANT 1 in Panax ginseng (PgBZR1) and brassinosteroid response during storage root formation. International Journal of Molecular Sciences 21(24):9666
  11. Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S (2016) The cbfs triple mutants reveal the essential functions of CBF s in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytologist 212(2):345-353 https://doi.org/10.1111/nph.14088
  12. Jiang B, Shi Y, Zhang X, Xin X, Qi L, Guo H, Li J, Yang S (2017) PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proceedings of the National Academy of Sciences 114(32):E6695-E6702 https://doi.org/10.1073/pnas.1706226114
  13. Jo I-H, Lee J, Hong CE, Lee DJ, Bae W, Park S-G, Ahn YJ, Kim YC, Kim JU, Lee JW (2017) Isoform sequencing provides a more comprehensive view of the Panax ginseng transcriptome. Genes 8(9):228
  14. Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of A rabidopsis. The Plant Journal 75(3):364-376 https://doi.org/10.1111/tpj.12205
  15. Kim YS, Lee M, Lee J-H, Lee H-J, Park C-M (2015) The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant molecular biology 89:187-201 https://doi.org/10.1007/s11103-015-0365-3
  16. Lee C-M, Thomashow MF (2012) Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 109(37):15054-15059
  17. Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017) MPK3-and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Developmental cell 43(5):630-642. e634 https://doi.org/10.1016/j.devcel.2017.09.025
  18. Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant physiology 119(2):463-470 https://doi.org/10.1104/pp.119.2.463
  19. Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proceedings of the National Academy of Sciences 101(11):3985-3990 https://doi.org/10.1073/pnas.0303029101
  20. Provart NJ, Gil P, Chen W, Han B, Chang H-S, Wang X, Zhu T (2003) Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant physiology 132(2):893-906 https://doi.org/10.1104/pp.103.021261
  21. Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. The Plant Cell 19(9):2749-2762
  22. Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends in plant science 23(7):623-637 https://doi.org/10.1016/j.tplants.2018.04.002
  23. Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. The Plant Cell 24(6):2578-2595 https://doi.org/10.1105/tpc.112.098640
  24. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proceedings of the National Academy of Sciences 95(24):14570-14575 https://doi.org/10.1073/pnas.95.24.14570
  25. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences 94(3):1035-1040 https://doi.org/10.1073/pnas.94.3.1035
  26. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular cell 15(1):141-152 https://doi.org/10.1016/j.molcel.2004.06.023
  27. Waminal NE, Pellerin RJ, Jang W, Kim HH, Yang T-J (2018) Characterization of chromosome-specific microsatellite repeats and telomere repeats based on low coverage whole genome sequence reads in Panax ginseng. Plant breeding and biotechnology 6(1):74-81 https://doi.org/10.9787/PBB.2018.6.1.74
  28. Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. The plant cell 14(suppl_1):S165-S183 https://doi.org/10.1105/tpc.000596
  29. Xu J, Chu Y, Liao B, Xiao S, Yin Q, Bai R, Su H, Dong L, Li X, Qian J (2017) Panax ginseng genome examination for ginsenoside biosynthesis. Gigascience 6(11):gix093
  30. Ye K, Li H, Ding Y, Shi Y, Song C, Gong Z, Yang S (2019) BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. The Plant Cell 31(11):2682-2696 https://doi.org/10.1105/tpc.19.00058
  31. Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a coldregulatory circuit that is desensitized by low temperature. Plant Physiology 133(2):910-918 https://doi.org/10.1104/pp.103.027169
  32. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu J-K (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant physiology 171(4):2744-2759 https://doi.org/10.1104/pp.16.00533