Plant Cell Reports

, Volume 38, Issue 9, pp 1181–1197 | Cite as

Effects of drought–re-watering–drought on the photosynthesis physiology and secondary metabolite production of Bupleurum chinense DC.

  • Linlin Yang
  • Yu Zhao
  • Qi Zhang
  • Lin Cheng
  • Mei Han
  • Yueying RenEmail author
  • Limin YangEmail author
Original Article


Key message

Drastic changes in soil water content can activate the short-term high expression of key enzyme-encoding genes involved in secondary metabolite synthesis thereby increasing the content of secondary metabolites.


Bupleurum chinense DC. is a traditional medicinal herb that is famous for its abundant saikosaponins. In the current study, the effects of drought–re-watering–drought on the photosynthesis physiology and biosynthesis of saikosaponins were investigated in 1-year-old B. chinense. The results showed that alterations in soil moisture altered the photosynthesis physiological process of B. chinense. The dry weight and fresh weight of the roots, photosynthesis capacity, chlorophyll fluorescence parameters, and SOD, POD and CAT activities were significantly reduced, and the contents of SP, soluble sugars, PRO and MDA increased. There were strong correlations between different physiological stress indices. All indices promoted and restricted each other, responded to soil moisture changes synergistically, maintained plant homeostasis and guaranteed normal biological activities. It was found that RW and RD_1 were the key stages of the water-control experiment affecting the expression of saikosaponin-related genes. At these two stages, the expression of multiple genes was affected by changes in soil moisture, with their expression levels reaching several-fold higher than those at the previous stage. We noticed that the expression of saikosaponin synthesis genes (which were rapidly upregulated at the RW and RD_1 stages) did not coincide with the rapid accumulation of saikosaponins (at the RD-2 stage), which were found to correspond to each other at the later stages of the water-control experiment. This finding indicates that there is a time lag between gene expression and the final product synthesis. Rapid changes in the external environment (RW to RD_1) have a short-term promoting effect on gene expression. This study reveals that short-term stress regulation may be an effective way to improve the quality of medicinal materials.


Bupleurum chinense DC. Drought stress Physiological changes Gene expression Saikosaponins 



This work was supported by China Agriculture Research System (Grant number CARS-21).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Batlang U, Baisakh N, Ambavaram MM, Pereira A (2013) Phenotypic and physiological evaluation for drought and salinity stress responses in rice. Methods Mol Biol 956:209–225CrossRefPubMedGoogle Scholar
  2. Bhargava S, Sawant K, Tuberosa R (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32CrossRefGoogle Scholar
  3. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91(Spec No):179–194CrossRefPubMedPubMedCentralGoogle Scholar
  4. Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40:4–10CrossRefPubMedGoogle Scholar
  5. Buschmann C (2007) Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynth Res 92:261–271CrossRefPubMedGoogle Scholar
  6. Centritto M, Brilli F, Fodale R, Loreto F (2011) Different sensitivity of isoprene emission, respiration and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra) saplings. Tree Physiol 31:275–286CrossRefPubMedGoogle Scholar
  7. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560CrossRefPubMedGoogle Scholar
  8. Cheng L, Han M, L-m Yang, Li Y, Sun Z, Zhang T (2018) Changes in the physiological characteristics and baicalin biosynthesis metabolism of Scutellaria baicalensis Georgi under drought stress. Ind Crops Prod 122:473–482CrossRefGoogle Scholar
  9. Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28CrossRefPubMedGoogle Scholar
  10. Deans RM, Brodribb TJ, Busch FA, Farquhar GD (2019) Plant water-use strategy mediates stomatal effects on the light induction of photosynthesis. New Phytol 222:382–395CrossRefPubMedGoogle Scholar
  11. Dubey VS, Bhalla R, Luthra R (2003) An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants. J Biosci 28:637–646CrossRefPubMedGoogle Scholar
  12. Ge Y, He X, Wang J, Jiang B, Ye R, Lin X (2014) Physiological and biochemical responses of Phoebe bournei seedlings to water stress and recovery. Acta Physiol Plant 36:1241–1250CrossRefGoogle Scholar
  13. Hayano-Kanashiro C, Calderon-Vazquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J (2009) Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS One 4:e7531CrossRefPubMedPubMedCentralGoogle Scholar
  14. Haznagy-Radnai E, Czigle S, Zupko I, Falkay G, Mathe I (2006) Comparison of antioxidant activity in enzyme-independent system of six Stachys species. Fitoterapia 77:521–524CrossRefPubMedGoogle Scholar
  15. He F, Sheng M, Tang M (2017) Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front Plant Sci 8:183PubMedPubMedCentralGoogle Scholar
  16. Huang HQ, Zhang X, Lin M, Shen YH, Yan SK, Zhang WD (2008) Characterization and identification of saikosaponins in crude extracts from three Bupleurum species using LC-ESI-MS. J Sep Sci 31:3190–3201CrossRefPubMedGoogle Scholar
  17. Jin R, Wang Y, Liu R, Gou J, Chan Z (2015) Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Front Plant Sci 6:1123CrossRefPubMedGoogle Scholar
  18. Khabibullaev PK, Zakhidov EA, Zakhidova MA, Kasymdzhanov MA, Nematov ShK, Abdukarimov AA, Nabiev SM, Saakova NA, Stamp P, Fracheboud I (2003) Evaluation of the effects of drought on cotton plants using characteristics of chlorophyll fluorescence. Dokl Biol Sci 392:442–444CrossRefPubMedGoogle Scholar
  19. Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci USA 97:13172–13177CrossRefPubMedGoogle Scholar
  20. Lee MH, Jeong JH, Seo JW, Shin CG, Kim YS, In JG, Yang DC, Yi JS, Choi YE (2004) Enhanced triterpene and phytosterol biosynthesis in Panax ginseng overexpressing squalene synthase gene. Plant Cell Physiol 45:976–984CrossRefPubMedGoogle Scholar
  21. Lin WY, Chen LR, Lin TY (2008) Rapid authentication of Bupleurum species using an array of immobilized sequence-specific oligonucleotide probes. Planta Med 74:464–469CrossRefPubMedGoogle Scholar
  22. Lin TY, Chiou CY, Chiou SJ (2013) Putative genes involved in saikosaponin biosynthesis in Bupleurum species. Int J Mol Sci 14:12806–12826CrossRefPubMedPubMedCentralGoogle Scholar
  23. Liu C, Liu Y, Guo K, Fan D, Li G, Zheng Y, Yu L, Yang R (2011a) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183CrossRefGoogle Scholar
  24. Liu H, Wang X, Wang D, Zou Z, Liang Z (2011b) Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge. Ind Crops Prod 33:84–88CrossRefGoogle Scholar
  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lu S, Peng X, Guo Z, Zhang G, Wang Z, Wang C, Pang C, Fan Z, Wang J (2007) In vitro selection of salinity tolerant variants from triploid bermudagrass (Cynodon transvaalensis × C. dactylon) and their physiological responses to salt and drought stress. Plant Cell Rep 26:1413–1420CrossRefPubMedGoogle Scholar
  27. Massacci A, Nabiev SM, Pietrosanti L, Nematov SK, Chernikova TN, Thor K, Leipner J (2008) Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiol Biochem 46:189–195CrossRefPubMedGoogle Scholar
  28. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefPubMedPubMedCentralGoogle Scholar
  29. Meng LS (2018) Compound synthesis or growth and development of roots/stomata regulate plant drought tolerance or water use efficiency/water uptake efficiency. J Agric Food Chem 66:3595–3604CrossRefPubMedGoogle Scholar
  30. Mitra S, Irshad M, Debnath B, Lu X, Li M, Dash CK, Rizwan HM, Qiu Z, Qiu D (2018) Effect of vineyard soil variability on chlorophyll fluorescence, yield and quality of table grape as influenced by soil moisture, grown under double cropping system in protected condition. PeerJ 6:e5592CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405CrossRefPubMedGoogle Scholar
  32. Mitton JB, Grant MC, Yoshino AM (1998) Variation in allozymes and stomatal size in pinyon (Pinus edulis, Pinaceae), associated with soil moisture. Am J Bot 85:1262–1265CrossRefPubMedGoogle Scholar
  33. Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 61:291–315CrossRefPubMedGoogle Scholar
  34. Monti A, Brugnoli E, Scartazza A, Amaducci MT (2006) The effect of transient and continuous drought on yield, photosynthesis and carbon isotope discrimination in sugar beet (Beta vulgaris L.). J Exp Bot 57:1253–1262CrossRefPubMedGoogle Scholar
  35. Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973CrossRefPubMedGoogle Scholar
  36. Nilsen ET, Freeman J, Grene R, Tokuhisa J (2014) A rootstock provides water conservation for a grafted commercial tomato (Solanum lycopersicum L.) line in response to mild-drought conditions: a focus on vegetative growth and photosynthetic parameters. PLoS One 9:e115380CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nolan RH, Tarin T, Santini NS, McAdam SAM, Ruman R, Eamus D (2017) Differences in osmotic adjustment, foliar abscisic acid dynamics, and stomatal regulation between an isohydric and anisohydric woody angiosperm during drought. Plant Cell Environ 40:3122–3134CrossRefPubMedGoogle Scholar
  38. Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plant 137:188–199CrossRefPubMedGoogle Scholar
  39. Ramachandra Reddy A, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202CrossRefPubMedGoogle Scholar
  40. Rogerio AP, Sa-Nunes A, Faccioli LH (2010) The activity of medicinal plants and secondary metabolites on eosinophilic inflammation. Pharmacol Res 62:298–307CrossRefPubMedGoogle Scholar
  41. Seki H, Tamura K, Muranaka T (2015) P450s and UGTs: key players in the structural diversity of triterpenoid saponins. Plant Cell Physiol 56:1463–1471CrossRefPubMedGoogle Scholar
  42. Selmar D, Kleinwächter M (2013) Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants. Ind Crops Prod 42:558–566CrossRefGoogle Scholar
  43. Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494CrossRefPubMedGoogle Scholar
  44. Singh B, Sharma RA (2015) Plant terpenes: defense responses, phylogenetic analysis, regulation and clinical applications. 3 Biotech 5:129–151CrossRefPubMedGoogle Scholar
  45. Sui C, Zhang J, Wei J, Chen S, Li Y, Xu J, Jin Y, Xie C, Gao Z, Chen H, Yang C, Zhang Z, Xu Y (2011) Transcriptome analysis of Bupleurum chinense focusing on genes involved in the biosynthesis of saikosaponins. BMC Genom 12:539CrossRefGoogle Scholar
  46. Tan LL, Cai X, Hu ZH, Ni XL (2008) Localization and dynamic change of saikosaponin in root of Bupleurum chinense. J Integr Plant Biol 50:951–957CrossRefPubMedGoogle Scholar
  47. Wang X, Feng Q, Xiao Y, Li P (2015) Radix Bupleuri ameliorates depression by increasing nerve growth factor and brain-derived neurotrophic factor. Int J Clin Exp Med 8:9205–9217PubMedPubMedCentralGoogle Scholar
  48. Wu S, Hu C, Tan Q, Nie Z, Sun X (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol Biochem 83:365–374CrossRefPubMedGoogle Scholar
  49. Yadav RK, Sangwan RS, Sabir F, Srivastava AK, Sangwan NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83CrossRefPubMedGoogle Scholar
  50. Yang C (2016) Adaptive plant physiology in extreme environments. J Plant Physiol 194:1CrossRefPubMedGoogle Scholar
  51. Yang ZY, Chao Z, Huo KK, Xie H, Tian ZP, Pan SL (2007) ITS sequence analysis used for molecular identification of the Bupleurum species from northwestern China. Phytomedicine 14:416–423CrossRefPubMedGoogle Scholar
  52. Zhu Z, Liang Z, Han R (2009a) Saikosaponin accumulation and antioxidative protection in drought-stressed Bupleurum chinense DC. plants. Environ Exp Bot 66:326–333CrossRefGoogle Scholar
  53. Zhu Z, Liang Z, Han R, Je Dong (2009b) Growth and saikosaponin production of the medicinal herb Bupleurum chinense DC. under different levels of nitrogen and phosphorus. Ind Crops Prod 29:96–101CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Cultivation Base of State Key Laboratory for Ecological Restoration and Ecosystem Management of Jilin Province, Ministry of Science and Technology, College of Chinese Medicinal MaterialsJilin Agricultural UniversityChangchunPeople’s Republic of China

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