Skip to main content

Advertisement

Springer Nature Link
Log in

Cell shape can be uncoupled from formononetin induction in a novel cell line from Callerya speciosa

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

It is the first time that formononetin produced by cell culture and its accumulation was shown to be triggered by specific stress signalling linked jasmonate pathway.

Abstract

Callerya speciosa, an endangered traditional Chinese medicine plant, is intensively used in traditional folk medicine. To develop sustainable alternatives for the overexploitation of natural resources, a suspension cell line was created from C. speciosa. Ingredients of C. speciosa, for instance the isoflavone formononetin, are formed during a peculiar swelling response of the root, which is considered as a quality trait for commercial application. A cell strain with elongated cells was obtained by using synthetic cytokinin 6-benzylaminopurine (6-BA) and synthetic auxin picloram. Both, picloram and 6-BA, promote cell division, whereas picloram was shown to be crucial for the maintenance of axial cell expansion. We addressed the question, whether the loss of axiality observed in the maturating root is necessary and sufficient for the accumulation of formononetin. While we were able to mimic a loss of axiality for cell expansion, either by specific combinations of 6-BA and picloram, or by treatment with the anti-microtubular compound oryzalin, formononetin was not detectable. However, formononetin could be induced by the stress hormone methyl jasmonate (MeJA), as well as by the bacterial elicitor flagellin peptide (flg22), but not by a necrosis inducing protein. Combined the fact that none of these treatments induced the loss of axiality, we conclude that formononetin accumulates in response to basal defence and unrelated with cell swelling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Ahmed ABA, Rao AS, Rao MV, Taha RM (2011) Effect of picloram, additives and plant growth regulators on somatic embryogenesis of Phyla nodiflora (L.) Greene. Braz Arch Biol Techn 54(1):7–13

    Article  CAS  Google Scholar 

  • Arens H, Ulbrich B, Fischer H, Parnham MJ, Römer A (1986) Novel antiinflammatory flavonoids from Podophyllum versipelle cell culture. Planta Med 52(6):468–473

    Article  Google Scholar 

  • Bannigan A, Wiedemeier AMD, Williamson RE, Overall RL, Baskin TI (2006) Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47(7):949–958

    Article  CAS  PubMed  Google Scholar 

  • Baskin TI (2015) Auxin inhibits expansion rate independently of cortical microtubules. Trends Plant Sci 20(8):471–472

    Article  CAS  PubMed  Google Scholar 

  • Baskin TI, Beemster GTS, Judy-March JE, Marga F (2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiol 135(4):2279–2290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bianco MD, Kepinski S (2011) Context, specificity, and self-organization in auxin response. Cold Spring Harbor Perspect Biol 3(1):a001578

    Google Scholar 

  • Bringi V, Kadkade P, Prince CL, Roach BL (2013) Enhanced production of paclitaxel and taxanes by cell cultures of Taxus species. U.S. Patent, 20130017582A1

  • Campanoni P, Nick P (2005) Auxin-dependent cell division and cell elongation: NAA and 2, 4-D activate different pathways. Plant Physiol 137(3):939–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang X, Nick P (2011) Defence signaling triggered by Flg22 and Harpin is integrated into a different stilbene output in Vitis cells. PLoS One 7(7):e40446

    Article  Google Scholar 

  • Chang X, Heene E, Qiao F, Nick P (2011) The Phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. Plos One 6(10):e26405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang X, Seo M, Takebayashi Y, Kamiya Y, Riemann M, Nick P (2017) Jasmonates are induced by the PAMP flg22 but not the cell death-inducing elicitor Harpin in Vitis rupestris. Protoplasma 254:271–283

    Article  CAS  PubMed  Google Scholar 

  • Eisinger WR, Morré DJ (1971) Growth-regulating properties of picloram, 4-amino-3, 5, 6-trichloropicolinic acid. Can J Bot 49(6):889–897

    Article  CAS  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18(3):265–276

    Article  CAS  PubMed  Google Scholar 

  • Frense D (2007) Taxianes: perspectives for biotechnological production. Appl Microbiol Biot 73(6):1233–1240

    Article  CAS  Google Scholar 

  • Furmanowa M, Glowniak K, Syklowska-Baranek K, Zgórka G, Józefczyk A (1997) Effect of picloram and methyl jasmonate on growth and taxane accumulation in callus culture of Taxus × media var. Hatfieldii. Plant Cell Tiss Org 49(1):75–79

    Article  CAS  Google Scholar 

  • Gijzen M, Nürnberger T (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochem 67(16):1800–1807

    Article  CAS  Google Scholar 

  • Green PB (1980) Organogenesis—a biophysical view. Annu Rev Plant Bio 31(1):51–82

    Article  Google Scholar 

  • Groll J, Mycock DJ, Gray VN, Laminski S (2001) Secondary somatic embryogenesis of cassava on picloram supplemented media. Plant Cell Tiss Org 65(3):201–210

    Article  CAS  Google Scholar 

  • He K (1711) Sheng Cao Yao Xing Bei Yao (medical characteristics of raw herb). Reprint by Gongdong Sci-Tech press, Guangzhou (2009) (in Chinese)

    Google Scholar 

  • Huang B, Xu L, Li Z, MA Q, Li K, Chen W (2008) Study on Tissue Culture Techniques for Stem Segment of Millettia speciosa Champ. Journal of Anhui Agriculture Science 36(32):13993–13994 (in Chinese)

    CAS  Google Scholar 

  • Imseng N. Schillberg S, Schürch C, Schmid D, Schütte K, Gorr G, Eibl D, Eibl R (2014) Suspension culture of plant cells under heterotrophic conditions. In: Meyer HP, Schmidhalter DR, eds. Industrial Scale Suspension Culture of Living Cells. Wiley-VCH Verlag GmbH & Co KGaA 123: 224–257

    Google Scholar 

  • Ismail A, Takeda S, Nick P (2014) Life and death under salt stress: same players, different timing? J Exp Bot 65(12):2963–2979

    Article  CAS  PubMed  Google Scholar 

  • Koda Y, Kikuta Y, Tazaki H, Tsujino Y, Sakamura S, Yoshihara T (1991) Potato tuber-inducing activities of jasmonic acid and related compounds. Phytochemistry 30(5):1435–1438

    Article  CAS  Google Scholar 

  • Kolewe ME, Gaurav V, Roberts SC (2008) Pharmaceutically active natural product synthesis and supply via plant cell culture technology. Mol Pharmaceut 5(2):243–256

    Article  CAS  Google Scholar 

  • Li SH, Dang YY, Zhou XL, Huang B, Huang XH, Zhang ZR, Kwan YW, Chan ShW, Leung GPH, Lee SMY, Hoi MPM (2015) Formononetin promotes angiogenesis through the estrogen receptor alpha-enhanced ROCK pathway. Nature Sci Rep 5:16815

    Article  CAS  Google Scholar 

  • Li J, Li C, Gou J, Wang X, Fan R, Zhang Y (2016) An Alternative Pathway for Formononetin Biosynthesis in Pueraria lobata. Front Plant Sci 7:861

    PubMed  PubMed Central  Google Scholar 

  • Lloyd C, Chan J (2008) The parallel lives of microtubules and cellulose microfibrils. Curr Opin Plant Biol 11(6):641–646

    Article  CAS  PubMed  Google Scholar 

  • Maisch J, Nick N (2007) Actin Is Involved in Auxin-Dependent Patterning. Plant Physiol 143(4):1695–1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacognosy Rev 1(1):69–79

    CAS  Google Scholar 

  • Nick P (2012) Microtubules and the tax payer. Protoplasma 249(Suppl. 2):S81–S94

    Article  PubMed  Google Scholar 

  • Nick P, Furuya M, Schäfer E (1991) Do microtubules control growth during tropism? Experiments with maize coleoptiles. Plant Cell Physiol 32(7):999–1006

    Article  Google Scholar 

  • Nick P, Ehmann B, Furuya M, Schäfer E (1993) Cell communication, stochastic cell responses, and anthocyanin pattern in mustard cotyledons. Plant Cell 5(5):541–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 6:1077

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito K, Matsuda F (2010) Metabolomics for functional genomics, systems biology, and biotechnology. Annu Rev Plant Biol 61(1):463–489

    Article  CAS  PubMed  Google Scholar 

  • Sharma M, Sharma A, Kumar A, Basu SK (2011) Enhancement of secondary metabolites in cultured plant cells through stress stimulus. Am J Plant Physiol 6(2):50–71

    Article  CAS  Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: Alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45(1):527–544

    Article  CAS  Google Scholar 

  • Smalle J, Van Der Straeten D (1997) Ethylene and vegetative development. Physiol Plantarum 100(3):593–605

    Article  CAS  Google Scholar 

  • Steinitz B, Bergfeld R (1977) Pattern formation underlying phytochrome-mediated anthocyanin synthesis in the cotyledons of Sinapis alba L. Planta 133(3):229–235

    Article  CAS  PubMed  Google Scholar 

  • Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64(5):874–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uchiyama T, Furukawa M, Isobe S (2003) New oleanane-type triterpene saponins from Millettia speciosa. Heterocycles 60(3):655–661

    Article  CAS  Google Scholar 

  • Valverde R, Arias O, Thorpe TA (1987) Picloram-induced somatic embryogenesis in pejibaye palm (Bactris gasipaes H.B.K.). Plant Cell Tiss Org 10(2):149–156

    Article  CAS  Google Scholar 

  • Walsh TA, Neal R, Merlo AO, Honma M, Hicks GR, Wolff K, Matsumura W, Davies JP (2006) Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2, 4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol 142(2):542–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Lai F, Wang M, Wang J (2011) Chemical Constituents of the roots of Millettia speciosa. Chin J Tropical Crops 32(12):2378–2380 (in Chinese)

    Google Scholar 

  • Wang M, Lai F, Wang J, Yan X, Wang Z (2013) Chemical constituents from the vinestems of Millettia speciosa. Nat Product Res Dev 25:53–55 (in Chinese)

    Google Scholar 

  • Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54(1):691–722

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An Update to the 2007 review in Annals of Botany. Ann Bot 111(6):1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson SA, Roberts SC (2012) Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotechnol J 10(3):249–268

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Zhang D, Yu F, Hao H, Li S (2015) Quality evaluate of Millettia speciosa champ. Pharmacy Today 25(2):90–92 (in Chinese)

    Google Scholar 

  • Xu L, Wang JB, Lei M, Li L, Fu YL, Wang ZN, Ao MF, Li ZhY (2016) Transcriptome Analysis of Storage Roots and Fibrous Roots of the Traditional Medicinal Herb Callerya speciosa (Champ.) ScHot. PLoS One 11(8):e0160338

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Sato F (1981) Production of berberine in cultured cells of Coptis japonica. Phytochemistry 20(3):545–547

    Article  CAS  Google Scholar 

  • Yeoman MM, Yeoman CL (1996) Manipulating secondary metabolism in cultured plant cells. New Phytol 134(4):553–569

    Article  CAS  Google Scholar 

  • Yukimune Y, Tabata H, Higashi Y, Hara Y (1996) Methyl jasmonate induced overproduction of paclitaxel and baccatin III in Taxus cell suspension cultures. Nat Biotechnol 14(9):1129–1132

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Yin T, Ling X, Liang H, Zhao Y (2008) Interactions between thrombin and natural products of Millettia speciosa Champ. using capillary zone electrophoresis. Electrophoresis 29(12):3391–3397

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Zhu W, Hu Q (2001) Enhanced catharanthine production in Catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Tech 22(6):673–681

    Article  CAS  Google Scholar 

  • Zheng Y (2009) Studies on extract techniques and pharmacological activities of polysaccharide from Millettia Speciosa Champ. [Master’s Thesis]. Jinan University (in Chinese)

  • Zong X, Lai Z, Wang Z, Wang J (2009) Studies on chemical constituents of root of Millettia speciosa. J Chin Med Mater 32(4):520–521 (in Chinese)

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Projects for Sino-German Cooperation on Agricultural Science and Technology (2014–2015) ‘Modernization of Traditional Chinese Medicine—A cell engineering technology of rare and precious medicinal plants’ and the Fundamental Scientific Research Funds for CATAS-TCGRI (1630032015022). We thank Prof. Dr. Zhiying Li for generating calli from stem of C. speciosa.

Author information

Authors and Affiliations

  1. Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture/Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, Hainan, 517317, People’s Republic of China

    Fei Qiao, Han-qing Cong, Hua-peng Sun & Li Li

  2. Hainan Key Laboratory of Sustainable Utilization of Tropical Bioresources/Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan, 570228, People’s Republic of China

    Xue-fei Jiang

  3. Molecular Cell Biology, Botanical Institute, Karlsruhe Institute of Technology, Fritz-Haber-Weg 4, 76131, Karlsruhe, Germany

    Peter Nick

Authors
  1. Fei Qiao
    View author publications

    Search author on:PubMed Google Scholar

  2. Xue-fei Jiang
    View author publications

    Search author on:PubMed Google Scholar

  3. Han-qing Cong
    View author publications

    Search author on:PubMed Google Scholar

  4. Hua-peng Sun
    View author publications

    Search author on:PubMed Google Scholar

  5. Li Li
    View author publications

    Search author on:PubMed Google Scholar

  6. Peter Nick
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Hua-peng Sun.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Kathryn K. Kamo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiao, F., Jiang, Xf., Cong, Hq. et al. Cell shape can be uncoupled from formononetin induction in a novel cell line from Callerya speciosa. Plant Cell Rep 37, 665–676 (2018). https://doi.org/10.1007/s00299-018-2259-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-018-2259-8

Keywords