ALGAE

  • 제39권3호
  • /
  • Pages.207-222
  • /
  • 2024
  • /
  • 1226-2617(pISSN)
  • /
  • 2093-0860(eISSN)
한국조류학회(藻類) (The Korean Society of Phycology)
권호 표지
DOI QR코드

DOI QR Code

Improving antistress capacity and lipid productivity in the green alga Chlorella pyrenoidosa by adding abscisic acid under salt stress conditions

  • Ke Ding (Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University) ;
  • Zheng Chen (Department of Dermatology, Shapingba Hospital, Chongqing University) ;
  • Qiwu Wan (Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University) ;
  • Xiaolin Hu (Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University) ;
  • Xiaohui Wang (Department of Oncology, Chongqing University Jiangjin Hospital) ;
  • Heng Li (Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University) ;
  • Yongzhong Wang (Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University) ;
  • Yang Luo (Department of Laboratory Medicine, Chongqing General Hospital, School of Medicine, Chongqing University) ;
  • Debing Xiang (Department of Oncology, Chongqing University Jiangjin Hospital)
  • 투고 : 2024.03.06
  • 심사 : 2024.08.28
  • 발행 : 2024.09.23
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

In this study, the regulation of abscisic acid (ABA) on cell growth and lipid biosynthesis was investigated under salt-induced stress in Chlorella pyrenoidosa. It is found that as suffering from only salt stress, although the lipid content of single cell was improved, the inhibitory effects of stress on cell proliferation was visible. When the algal cells were exposed to salt stress and ABA conditions, lipid productivity was increased (45.35 mg L-1 d-1) by 1.17-fold compared to that of control cells (20.91 mg L-1 d-1), and the inhibition to cell growth was relieved. Transcriptomic analysis revealed that after adding ABA, these genes involved in antioxidant activity, jasmonic acid (JA) biosynthesis, and lipid biosynthesis were upregulated. Subsequently, we observed that the levels of glutathione, total antioxidant capacity, trehalose, and JA were elevated and the levels of reactive oxygen species were reduced. This study presents an effective approach to improve lipid production in algal cells, a new mechanism on that ABA alleviates intracellular oxidative stress through JA signaling pathway was elaborated.

키워드

과제정보

This work was supported by the National Natural Science Foundation of China (Grant No. 82241059), Chongqing Postdoctoral Science Foundation (Grant Nos. CSTB2022NSCQ-BHX0703, CSTB2022NSCQ-BHX0717), National Key Research and Development Program (Grant No. 2022YFC2009600), Program for Postgraduate Tutor Team Building of Chongqing (Grant No. YDSTD1924), and the Fundamental Research Funds for the Central Universities (Grant Nos. 2022CDJQY-002, 2023CDJYGRH-YB15).

참고문헌

  1. Adie, B. A. T., Perez-Perez, J., Perez-Perez, M. M., et al. 2007. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665-1681. doi.org/10.1105/tpc.106.048041
  2. Ali, M. S. & Baek, K.-H. 2020. Jasmonic acid signaling pathway in response to abiotic stresses in plants. Int. J. Mol. Sci. 21:621. doi.org/10.3390/ijms21020621
  3. Anjum, N. A., Ahmad, I., Mohmood, I., et al. 2012. Modulation of glutathione and its related enzymes in plants' responses to toxic metals and metalloids: a review. Environ. Exp. Bot. 75:307-324. doi.org/10.1016/j.envexpbot.2011.07.002
  4. Ben Rejeb, K., Abdelly, C. & Savoure, A. 2014. How reactive oxygen species and proline face stress together. Plant Physiol. Biochem. 80:278-284. doi.org/10.1016/j.plaphy.2014.04.007
  5. Cao, Y., Li, K., Li, Y., Zhao, X. & Wang, L. 2020. MYB transcription factors as regulators of secondary metabolism in plants. Biology 9:61. doi.org/10.3390/biology9030061
  6. Chae, H., Kim, E. J., Kim, H. S., Choi, H.-G., Kim, S. & Kim, J. H. 2023. Morphology and phylogenetic relationships of two Antarctic strains within the genera Carolibrandtia and Chlorella (Chlorellaceae, Trebouxiophyceae). Algae 38:241-252. doi.org/10.4490/algae. 2023.38.11.30
  7. Colina, F. J., Carbo, M., Jesus Canal, M. & Valledor, L. 2020. A complex metabolic rearrangement towards the accumulation of glycerol and sugars consequence of a proteome remodeling is required for the survival of Chlamydomonas reinhardtii growing under osmotic stress. Environ. Exp. Bot. 180:104261. doi.org/10.1016/j.envexpbot.2020.104261
  8. Ding, K., Wang, N., Huang, X., et al. 2020. Enhancing lipid productivity with novel SiO2-modified polytetrafluoroethylene (PTFE) membranes in a membrane photobioreactor. Algal Res. 45:101752. doi.org/10.1016/j.algal.2019.101752
  9. Eibl, R. H. & Schneemann, M. 2022. Cell-free DNA as a biomarker in cancer. Extracell. Vesicles Circ. Nucleic Acids 3:178-198. doi.org/10.20517/evcna.2022.20
  10. Fan, J., Ning, K., Zeng, X., et al. 2015. Genomic foundation of starch-to-lipid switch in oleaginous Chlorella spp. Plant Physiol. 169:2444-2461. doi.org/10.1104/pp.15.01174
  11. Guajardo, E., Correa, J. A. & Contreras-Porcia, L. 2016. Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243:767-781. doi.org/10.1007/s00425-015-2438-6
  12. Guo, Q., Liu, L., Rupasinghe, T. W. T., Roessner, U. & Barkla, B. J. 2022. Salt stress alters membrane lipid content and lipid biosynthesis pathways in the plasma membrane and tonoplast. Plant Physiol. 189:805-826. doi.org/10.1093/plphys/kiac123
  13. Islam, M. O., Kato, H., Shima, S., Tezuka, D., Matsui, H. & Imai, R. 2019. Functional identification of a rice trehalase gene involved in salt stress tolerance. Gene 685:42-49. doi.org/10.1016/j.gene.2018.10.071
  14. Ji, X., Cheng, J., Gong, D., et al. 2018. The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga: Scenedesmus obliquus XJ002. Sci. Total Environ. 633:593-599. doi.org/10.1016/j.scitotenv.2018.03.240
  15. Kasote, D. M., Jayaprakasha, G. K., Ong, K., Crosby, K. M. & Patil, B. S. 2020. Hormonal and metabolites responses in Fusarium wilt-susceptible and -resistant watermelon plants during plant-pathogen interactions. BMC Plant Biol. 20:481. doi.org/10.1186/s12870-020-02686-9
  16. Kim, M., Oh, H. J., Nguyen, K. & Jin, E. 2022. Identification and characterization of Dunaliella salina OH214 strain newly isolated from a saltpan in Korea. Algae 37:317-329. doi.org/10.4490/algae.2022.37.9.13
  17. Kou, Y., Liu, M., Sun, P., Dong, Z. & Liu, J. 2020. High light boosts salinity stress-induced biosynthesis of astaxanthin and lipids in the green alga Chromochloris zofingiensis. Algal Res. 50:101976. doi.org/10.1016/j.algal.2020.101976
  18. Kusvuran, S. 2021. Microalgae (Chlorella vulgaris Beijerinck) alleviates drought stress of broccoli plants by improving nutrient uptake, secondary metabolites, and anti-oxidative defense system. Hortic. Plant J. 7:221-231. doi.org/10.1016/j.hpj.2021.03.007
  19. Li, J., Xu, Y., Niu, Q., He, L., Teng, Y. & Bai, S. 2018. Abscisic acid (ABA) promotes the induction and maintenance of pear (Pyrus pyrifolia white pear group) flower bud endodormancy. Int. J. Mol. Sci. 19:310. doi.org/10.3390/ijms19010310
  20. Lin, B., Ahmed, F., Du, H., et al. 2018. Plant growth regulators promote lipid and carotenoid accumulation in Chlorella vulgaris. J. Appl. Phycol. 30:1549-1561. doi.org/10.1007/s10811-017-1350-9
  21. Norlina, R., Norashikin, M. N., Loh, S. H., Aziz, A. & Cha, T. S. 2020. Exogenous abscisic acid supplementation at early stationary growth phase triggers changes in the regulation of fatty acid biosynthesis in Chlorella vulgaris UMTM1. Appl. Biochem. Biotechnol. 191:1653-1669. doi.org/10.1007/s12010-020-03312-y
  22. Pretorius, C. J., Zeiss, D. R. & Dubery, I. A. 2021. The presence of oxygenated lipids in plant defense in response to biotic stress: a metabolomics appraisal. Plant Signal. Behav. 16:1989215. doi.org/10.1080/15592324.2021.1989215
  23. Qiao, T., Zhao, Y., Zhong, D.-b. & Yu, X. 2021. Hydrogen peroxide and salinity stress act synergistically to enhance lipids production in microalga by regulating reactive oxygen species and calcium. Algal Res. 53:102017. doi.org/10.1016/j.algal.2020.102017
  24. Rajasheker, G., Jawahar, G., Jalaja, N., et al. 2019. Role and regulation of osmolytes and ABA interaction in salt and drought stress tolerance. In Khan, M. I., Ferrante, A., Reddy, P. S. & Khan, N. A. (Eds.) Plant Signaling Molecules: Role and Regulations under Stressful Environments. Elsevier, Amsterdam, pp. 417-436. doi.org/10.1016/B978-0-12-816451-8.00026-5
  25. Reina-Bueno, M., Argandona, M., Nieto, J. J., et al. 2012. Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli. BMC Microbiol. 12:207. doi.org/10.1186/1471-2180-12-207
  26. Ren, C.-G. & Dai, C.-C. 2012. Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. BMC Plant Biol. 12:128. doi.org/10.1186/1471-2229-12-128
  27. Saddhe, A. A., Kundan, K. & Padmanabh, D. 2017. Mechanism of ABA signaling in response to abiotic stress in plants. In Pandey, G. K. (Ed.) Mechanism of Plant Hormone Signaling under Stress, Vol. 2. Wiley-Blackwell, Hoboken, NJ, pp. 173-195.
  28. Sakhno, L. O., Yemets, A. I. & Blume, Y. B. 2019. The role of ascorbate-glutathione pathway in reactive oxygen species balance under abiotic stresses. In Hasanuzzaman, M., Fotopoulos, V., Nahar, K. & Fujita, M. (Eds.) Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms. John Wiley & Sons, Hoboken, NJ, pp. 89-111.
  29. Song, X., Zhao, Y., Han, B., et al. 2020. Strigolactone mediates jasmonic acid-induced lipid production in microalga Monoraphidium sp. QLY-1 under nitrogen deficiency conditions. Bioresour. Technol. 306:123107. doi.org/10.1016/j.biortech.2020.123107
  30. Stirk, W. A. & van Staden, J. 2020. Potential of phytohormones as a strategy to improve microalgae productivity for biotechnological applications. Biotechnol. Adv. 44:107612. doi.org/10.1016/j.biotechadv.2020.107612
  31. Suparmaniam, U., Lam, M. K., Lim, J. W., et al. 2023. Influence of environmental stress on microalgae growth and lipid profile: a systematic review. Phytochem. Rev. 22:879-901. doi.org/10.1007/s11101-022-09810-7
  32. Tamaki, S., Mochida, K. & Suzuki, K. 2021. Diverse biosynthetic pathways and protective functions against environmental stress of antioxidants in microalgae. Plants (Basel) 10:1250. doi.org/10.3390/plants10061250
  33. Wang, C., Deng, Y., Liu, Z. & Liao, W. 2021a. Hydrogen sulfide in plants: crosstalk with other signal molecules in response to abiotic stresses. Int. J. Mol. Sci. 22:12068. doi.org/10.3390/ijms222112068
  34. Wang, C., Qi, M., Guo, J., et al. 2021b. The active phytohormone in microalgae: the characteristics, efficient detection, and their adversity resistance applications. Molecules 27:46. doi.org/10.3390/molecules27010046
  35. Wang, Y., Mostafa, S., Zeng, W. & Jin, B. 2021c. Function and mechanism of jasmonic acid in plant responses to abiotic and biotic stresses. Int. J. Mol. Sci. 22:8568. doi.org/10.3390/ijms22168568
  36. Wu, G., Gao, Z., Du, H., et al. 2018. The effects of abscisic acid, salicylic acid and jasmonic acid on lipid accumulation in two freshwater Chlorella strains. J. Gen. Appl. Microbiol. 64:42-49. doi.org/10.2323/jgam.2017.06.001
  37. Yang, L., Qiao, L., Su, X., Ji, B. & Dong, C. 2022. Drought stress stimulates the terpenoid backbone and triterpenoid biosynthesis pathway to promote the synthesis of saikosaponin in Bupleurum chinense DC. roots. Molecules 27:5470. doi.org/10.3390/molecules27175470
  38. Yang, Z.-Y., Huang, K.-X., Zhang, Y.-R., et al. 2023. Efficient microalgal lipid production driven by salt stress and phytohormones synergistically. Bioresour. Technol. 367:128270. doi.org/10.1016/j.biortech.2022.128270
  39. Yoshida, K., Igarashi, E., Mukai, M., Hirata, K. & Miyamoto, K. 2003. Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant Cell Environ. 26:451-457. doi.org/10.1046/j.1365-3040.2003.00976.x
  40. Zhang, L., Wang, N., Yang, M., et al. 2019. Lipid accumulation and biodiesel quality of Chlorella pyrenoidosa under oxidative stress induced by nutrient regimes. Renew. Energ. 143:1782-1790. doi.org/10.1016/j.renene.2019.05.081
  41. Zhang, L., Wang, Y.-Z., Wang, S. & Ding, K. 2018. Effect of carbon dioxide on biomass and lipid production of Chlorella pyrenoidosa in a membrane bioreactor with gasliquid separation. Algal Res. 31:70-76. doi.org/10.1016/j.algal.2018.01.014
  42. Zhao, Y., Wang, H.-P., Han, B. & Yu, X. 2019. Coupling of abiotic stresses and phytohormones for the production of lipids and high-value by-products by microalgae: a review. Bioresour. Technol. 274:549-556. doi.org/10.1016/j.biortech.2018.12.030
  43. Zhao, Y., Wang, H.-P., Yu, C., et al. 2021. Integration of physiological and metabolomic profiles to elucidate the regulatory mechanisms underlying the stimulatory effect of melatonin on astaxanthin and lipids coproduction in Haematococcus pluvialis under inductive stress conditions. Bioresour. Technol. 319:124150. doi.org/10.1016/j.biortech.2020.124150
  44. Zhao, Y., Wang, Q., Gu, D., et al. 2023. Melatonin, a phytohormone for enhancing the accumulation of high-value metabolites and stress tolerance in microalgae: applications, mechanisms, and challenges. Bioresour. Technol. 393:130093. doi.org/10.1016/j.biortech.2023.130093