Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Functional characterization of gibberellin signaling-related genes in Panax ginseng

  • Kim, Jinsoo (Department of Biology, Chungbuk National University) ;
  • Shin, Woo-Ri (Department of Biological Sciences and Biotechnology, Chungbuk National University) ;
  • Kim, Yang-Hoon (Department of Biological Sciences and Biotechnology, Chungbuk National University) ;
  • Shim, Donghwan (Department of Biological Sciences, Chungnam National University) ;
  • Ryu, Hojin (Department of Biology, Chungbuk National University)
  • Received : 2021.08.14
  • Accepted : 2021.09.17
  • Published : 2021.09.30
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Abstract

Gibberellins (GAs) are essential phytohormones for plant growth that influence developmental processes and crop yields. Recent functional genomic analyses of model plants have yielded good characterizations of the canonical GA signaling pathways and related genes. Although Panax ginseng has long been considered to have economic and medicinal importance, functional genomic studies of the GA signaling pathways in this crucial perennial herb plant have been rarely conducted. Here, we identified and performed functional analysis of the GA signaling-related genes, including PgGID1s, PgSLY1s, and PgRGAs. We confirmed that the physiological role of GA signaling components in P. ginseng was evolutionarily conserved. In addition, the important functional domains and amino acid residues for protein interactions among active GA, GID1, SCFSLY1, and RGA were also functionally conserved. Prediction and comparison of crystallographic structural similarities between PgGID1s and AtGID1a supported their function as GA receptors. Moreover, the subcellular localization and GA-dependent promotion of DELLA degradation in P. ginseng was similar to the canonical GA signaling pathways in other plants. Finally, we found that overexpression of PgRGA2 and PgSLY1-1 was sufficient to complement the GA-related phenotypes of atgid1a/c double- and rga quintuple-mutants, respectively. This critical information for these GA signaling genes has the potential to facilitate future genetic engineering and breeding of P. ginseng for increased crop yield and production of useful substances.

Keywords

Acknowledgement

This research was supported by Chungbuk National University Korea National University Development Project (2020)

References

  1. Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. Journal of experimental botany 60(4):1085-1092 https://doi.org/10.1093/jxb/ern301
  2. Ariizumi T, Lawrence PK, Steber CM (2011) The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant physiology 155(2):765-775 https://doi.org/10.1104/pp.110.166272
  3. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant molecular biology 69(4):473-488 https://doi.org/10.1007/s11103-008-9435-0
  4. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131(5):1055-1064 https://doi.org/10.1242/dev.00992
  5. Dill A, Jung H-S, Sun T-p (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proceedings of the National Academy of Sciences 98(24):14162-14167 https://doi.org/10.1073/pnas.251534098
  6. Dill A, Sun T-p (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159(2):777-785 https://doi.org/10.1093/genetics/159.2.777
  7. Dill A, Thomas SG, Hu J, Steber CM, Sun T-p (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. The Plant Cell 16(6):1392-1405 https://doi.org/10.1105/tpc.020958
  8. Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. The Plant Cell 14(12):3191-3200 https://doi.org/10.1105/tpc.006197
  9. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-p (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. The Plant Cell 18(12):3399-3414 https://doi.org/10.1105/tpc.106.047415
  10. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an "inhibitor of an inhibitor" enables flexible response to fluctuating environments. The Plant Cell 21(5):1328-1339 https://doi.org/10.1105/tpc.109.066969
  11. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. The Plant Cell 19 (10):3058-3079
  12. Hong CP, Kim J, Lee J, Yoo S-i, Bae W, Geem KR, Yu J, Jang I-b, Jo IH, Cho H, Shim D, Ryu H (2021) Gibberellin signaling promotes the secondary growth of storaage roots in Panax ginseng. International Journal of Molecular Science 22:8694 https://doi.org/10.3390/ijms22168694
  13. Hong J, Kim H, Ryu H (2018) Identification of ABSCISIC ACID (ABA) signaling related genes in Panax ginseng. J Plant Biotechnology (45):306-314
  14. Hu SY (1976) The genusPanax (ginseng) in Chinese medicine. Economic Botany 30(1):11-28 https://doi.org/10.1007/BF02866780
  15. Jang H-J, Han I-H, Kim Y-J, Yamabe N, Lee D, Hwang GS, Oh M, Choi K-C, Kim S-N, Ham J (2014) Anticarcinogenic effects of products of heat-processed ginsenoside Re, a major constituent of ginseng berry, on human gastric cancer cells. Journal of agricultural and food chemistry 62(13):2830-2836 https://doi.org/10.1021/jf5000776
  16. Jo I-H, Lee J, Hong C, Lee D, Bae W, Park S-G, Ahn Y, Kim Y, Kim J, Lee J (2017) Isoform sequencing provides a more comprehensive view of the panax ginseng transcriptome. Genes 8(9):228 https://doi.org/10.3390/genes8090228
  17. King KE, Moritz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159(2):767-776 https://doi.org/10.1093/genetics/159.2.767
  18. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecu lar evolutionary genetics analysis version 7.0 for bigger datasets. Molecular biology and evolution 33(7):1870-1874 https://doi.org/10.1093/molbev/msw054
  19. Lee J, Kim H, Park SG, Hwang H, Yoo Si, Bae W, Kim E, Kim J, Lee HY, Heo TY (2021) Brassinosteroid-BZR1/2-WAT1 module determines the high level of auxin signalling in vascular cambium during wood formation. New Phytologist 230(4):1503-1516 https://doi.org/10.1111/nph.17265
  20. Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes & development 16(5):646-658 https://doi.org/10.1101/gad.969002
  21. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun T-p, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. The Plant Cell 15(5):1120-1130 https://doi.org/10.1105/tpc.010827
  22. Nelson SK, Steber CM (2018) Gibberellin hormone signal perception: down-regulating DELLA repressors of plant growth and development. Annual Plant Reviews online:153-187
  23. Olszewski N, Sun T-p, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. The Plant Cell 14 (suppl 1):S61-S80 https://doi.org/10.1105/tpc.010476
  24. Reid JB (1993) Plant hormone mutants. Journal of Plant Growth Regulation 12(4):207-226 https://doi.org/10.1007/BF00213038
  25. Ross JJ, Murfet IC, Reid JB (1997) Gibberellin mutants. Physiologia Plantarum 100(3):550-560 https://doi.org/10.1034/j.1399-3054.1997.1000317.x
  26. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong D-H, An G, Kitano H, Ashikari M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299(5614):1896-1898 https://doi.org/10.1126/science.1081077
  27. Seo E, Kim S, Lee S, Oh B-C, Jun H-S (2015) Ginseng berry extract supplementation improves age-related decline of insulin signaling in mice. Nutrients 7(4):3038-3053 https://doi.org/10.3390/nu7043038
  28. Sun T-p (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant physiology 154(2):567-570 https://doi.org/10.1104/pp.110.161554
  29. Sun T-p (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biology 21(9):R338-R345 https://doi.org/10.1016/j.cub.2011.02.036
  30. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-p (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant physiology 135(2):1008-1019 https://doi.org/10.1104/pp.104.039578
  31. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T-y, Yue-ie CH, Kitano H, Yamaguchi I (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437(7059):693 https://doi.org/10.1038/nature04028
  32. 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
  33. 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
  34. Yasukawa K, Whang W-K, Ko S-K (2016) Inhibitory effects of ginseng (Panax ginseng) berry on tumour promotion and inflammatory ear oedema induced by TPA. Journal of Nutritional Therapeutics 4(4):143-148 https://doi.org/10.6000/1929-5634.2015.04.04.6