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Inhibition of root growth by narciclasine is caused by DNA damage-induced cell cycle arrest in lettuce seedlings

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Abstract

Narciclasine (NCS) is an Amaryllidaceae alkaloid isolated from Narcissus tazetta bulbs. Its phytotoxic effects on plant growth were examined in lettuce (Lactuca sativa L.) seedlings. Results showed that high concentrations (0.5–5 μM) of NCS restricted the growth of lettuce roots in a dose-dependent manner. In NCS-treated lettuce seedlings, the following changes were detected: reduction of mitotic cells and cell elongation in the mature region, inhibition of proliferation of meristematic cells, and cell cycle. Moreover, comet assay and terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay indicated that higher levels NCS (0.5–5 μM) induced DNA damage in root cells of lettuce. The decrease in meristematic cells and increase in DNA damage signals in lettuce roots in responses to NCS are in a dose-dependent manner. NCS-induced reactive oxygen species accumulation may explain an increase in DNA damage in lettuce roots. Thus, the restraint of root growth is due to cell cycle arrest which is caused by NCS-induced DNA damage. In addition, it was also found that NCS (0.5–5 μM) inhibited the root hair development of lettuce seedlings. Further investigations on the underlying mechanism revealed that both auxin and ethylene signaling pathways are involved in the response of root hairs to NCS.

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Abbreviations

ACC:

1-aminocyclopropane-1-carboxylic acid

DAPI:

4′,6-diamidino-2-phenylindole

DCFH-DA:

2,7-dichlorofluorescin diacetate

H2O2 :

Hydrogen peroxide

HU:

Hydroxyurea

IAA:

Indole-3-acetic acid

LMP:

Low-melting-point

NCS:

Narciclasine

NMP:

Normal-melting-point

OTM:

Olive tail moment

O2− :

Superoxide ion

PBS:

Phosphate-buffered saline

ROS:

Reactive oxygen species

TUNEL:

Terminal deoxynucleotidyl transferase dUTP nick end labeling

References

  • Bastida J, Lavilla R, Viladomat F (2006) Chemical and biological aspects of Narcissus alkaloids. Alkaloids Chem Biol 3:87–179

    Article  Google Scholar 

  • Berkov S, Bastida J, Sidjimova B, Viladomat F, Codina C (2008) Phytochemical differentiation of Galanthus nivalis and Galanthus elwesii (Amaryllidaceae): a case study. Biochem Syst Ecol 36:638–645

    Article  CAS  Google Scholar 

  • Bi YR, Yung KH, Wong YH (1998) Physiological effects of narciclasine from the mucilage of Narcissus tazetta L. bulbs. Plant Sci 135:103–108

    Article  CAS  Google Scholar 

  • Bi YR, Zhang LX, Guo JK, Yung KH, Wong YS (2003) Narciclasine alters chloroplast membrane structure and inhibits 5-aminolevulinic acid and chlorophyll binding protein accumulation in wheat (Triticum aestivum) leaves. N Z J Crop Hortic Sci 31:335–343

    Article  CAS  Google Scholar 

  • Carrasco L, Fresno M, Vazquez D (1975) Narciclasine: an antitumour alkaloid which blocks peptide bond formation by eukaryotic ribosomes. FEBS Lett 52:236–239

    Article  CAS  PubMed  Google Scholar 

  • Ceriotti G (1967) Narciclasine: an antimitotic substance from Narcissus bulbs. Nature 213:595–596

    Article  CAS  PubMed  Google Scholar 

  • Charoenying P, Teerarak M, Laosinwattana C (2010) An allelopathic substance isolated from Zanthoxylum limonella Alston fruit. Sci Hortic 125:411–416

    Article  CAS  Google Scholar 

  • Cools T, De Veylder L (2008) DNA stress checkpoint control and plant development. Curr Opin Plant Biol 12:1–6

    Google Scholar 

  • Decordier I, Cundari E, Kirsch-Volders M (2008) Mitotic checkpoints and the maintenance of the chromosome karyotype. Mutat Res 651:3–13

    Article  CAS  PubMed  Google Scholar 

  • Den Boer BGW, Murray JAH (2000) Triggering the cell cycle in plants. Trends Cell Biol 10:245–250

    Article  Google Scholar 

  • Ding L, Qi L, Jing H, Li J, Wang W, Wang T (2008) Phytotoxic effects of leukamenin E (an ent-kaurene diterpenoid) on root growth and root hair development in Lactuca sativa L. seedlings. J Chem Ecol 34:1492–1500

    Article  CAS  PubMed  Google Scholar 

  • Ding L, Jing H, Qin B, Qi L, Li J, Wang T, Liu G (2010) Regulation of cell division and growth in roots of Lactuca sativa L. seedlings by the ent-kaurene diterpenoid rabdosin B. J Chem Ecol 36:553–563

    Article  CAS  PubMed  Google Scholar 

  • Doležel J, Cíhalíková J, Weiserová J, Lucretti S (1999) Cell cycle synchronization in plant root meristems. Methods Cell Sci 21:95–107

    Article  PubMed  Google Scholar 

  • Dumont P, Ingrassia L, Rouzeau S, Ribaucour F, Thomas S, Roland I, Darro F, Lefranc F, Kiss R (2007) The Amaryllidaceae isocarbostyril narciclasine induces apoptosis by activation of the death receptor and/or mitochondrial pathways in cancer cells but not in normal fibroblasts. Neoplasia 9:766–776

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Evidente A, Kornienko A (2009) Anticancer evaluation of structurally diverse Amaryllidaceae alkaloids and their synthetic derivates. Phytochem Rev 8:449–459

    Article  CAS  Google Scholar 

  • Fusconi A, Gallo C, Camusso W (2007) Effects of cadmium on root apical meristems of Pisum sativum L.: cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat Res 632:9–19

    Article  CAS  PubMed  Google Scholar 

  • Gabrielsen B, Monath TP, Huggins JW, Kefauver DF, Pettit GR, Groszek G, Hollingshead M, Kirsi JJ, Shannon WM, Schubert EM (1992) Antiviral (RNA) activity of selected Amaryllidaceae isoquinoline constituents and synthesis of related substances. J Nat Prod 55:1569–1581

    Article  CAS  PubMed  Google Scholar 

  • Gichner T, Patková Z, Száková J, Žnidar I, Mukherjee A (2008) DNA damage in potato plants induced by cadmium, ethyl methanesulphonate and γ-rays. Environ Exp Bot 62:113–119

    Article  CAS  Google Scholar 

  • Gniazdowska A, Bogatek R (2005) Allelopathic interactions between plants. Multi site action of allelochemicals. Acta Physiol Plant 27:395–407

    CAS  Google Scholar 

  • Hefner E, Huefner N, Britt AB (2006) Tissue-specific regulation of cell-cycle responses to DNA damage in Arabidopsis seedlings. DNA Repair 5:102–110

    Article  CAS  PubMed  Google Scholar 

  • Inderjit, Callaway RM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11

    Article  CAS  Google Scholar 

  • Jakoby M, Schnittger A (2004) Cell cycle and differentiation. Curr Opin Plant Biol 7:661–669

    Article  CAS  PubMed  Google Scholar 

  • Kekre N, Griffin C, McNulty J, Pandey S (2005) Pancratistatin causes early activation of caspase-3 and the flipping of phosphatidyl serine followed by rapid apoptosis specifically in human lymphoma cells. Cancer Chemother Pharmacol 56:29–38

    Article  CAS  PubMed  Google Scholar 

  • Końca K, Lankoff A, Banasik A, Lisowska H, Kuszewski T, Góźdź S, Koza Z, Wojcik A (2003) A cross-platform public domain PC image-analysis program for the comet assay. Mutat Res 534:15–20

    Article  PubMed  Google Scholar 

  • Kong CH, Hu F, Xu XH (2002) Allelopathic potential and chemical constituents of volatiles from Ageratum conyzoides under stress. J Chem Ecol 28:1173–1182

    Article  CAS  PubMed  Google Scholar 

  • Kornienko A, Evidente A (2008) Chemistry, biology, and medicinal potential of narciclasine and its congeners. Chem Rev 108:1982–2014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lefranc F, Sauvage S, Goietsenoven GV, Mégalizzi V, Lamoral-Theys D, Debeir O, Spiegl-Kreinecker S, Berger W, Mathieu V, Decaestecker C, Kiss R (2009) Narciclasine, a plant growth modulator, activates Rho and stress fibers in glioblastoma cells. Mol Cancer Ther 8:1739–1750

    Article  CAS  PubMed  Google Scholar 

  • Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2:1071–1080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu W, Yang YS, Li P, Zhou Q, Sun T (2004) Root growth inhibition and induction of DNA damage in soybean (Glycine max) by chlorobenzenes in contaminated soil. Chemosphere 57:101–106

    Article  CAS  PubMed  Google Scholar 

  • Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8:1505–1517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Na X, Hu Y, Yue K, Lu H, Jia P, Wang H, Wang X, Bi Y (2011) Concentration-dependent effects of narciclasine on cell cycle progression in Arabidopsis root tips. BMC Plant Biol 11:184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oracz K, Bailly C, Gniazdowska A, Come D, Corbineau F, Bogatek R (2007) Induction of oxidative stress by sunflower phytotoxins in germinating mustard seeds. J Chem Ecol 33:251–264

    Article  CAS  PubMed  Google Scholar 

  • Pearson VE (2001) Galantamine: a new Alzheimer drug with a past life. Ann Pharmacother 35:1406–1413

    Article  CAS  PubMed  Google Scholar 

  • Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A, Vandepoele K, Magyar Z, Hatzfeld Y, Van Der Schueren E, Beemster GTS (2007) Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J Biol Chem 282:25588–25596

    Article  CAS  PubMed  Google Scholar 

  • Piozzi F, Marino ML, Fuganti C, Martino AD (1969) Occurrence of non-basic metabolites in Amaryllidaceae. Phytochemistry 8:1745–1748

    Article  CAS  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560

    Article  CAS  PubMed  Google Scholar 

  • Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28–45

    Article  PubMed Central  PubMed  Google Scholar 

  • Roldán-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169–179

    Article  PubMed  Google Scholar 

  • Sánchez-Moreiras AM, de la Pena TB, Reigosa MJ (2008) The natural compound benzoxazolin-2(3H)-one selectively retards cell cycle in lettuce root meristems. Phytochemistry 69:2172–2179

    Article  PubMed  Google Scholar 

  • Sánchez-Moreiras AM, Martínez-Peňalver A, Reigosa MJ (2011) Early senescence induced by 2-3H-benzoxazolinone (BOA) in Arabidopsis thaliana. J Plant Phsiol 168:863–870

    Google Scholar 

  • Soltys D, Rudzińska-Langwald A, Kurek W, Gniazdowska A, Sliwinska E, Bogatek R (2011) Cyanamide mode of action during inhibition of onion (Allium cepa L.) root growth involves disturbances in cell division and cytoskeleton formation. Planta 234:609–621

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Teerarak M, Charoenying P, Laosinwattana C (2012) Physiological and cellular mechanisms of natural herbicide resource from Aglaia odorata Lour. on bioassay plants. Acta Physiol Plant. doi:10.1007/s11738-011-0923-5

    Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    Google Scholar 

  • Vanderauwera S, Suzuki N, Miller G, van de Cotte B, Morsa S, Ravanat JL, Hegie A, Triantaphylidès C, Shulaev V, Van Montagu MC, Van Breusegem F, Mittler R (2011) Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci U S A 4:1711–1716

    Article  Google Scholar 

  • Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479

    Article  CAS  PubMed  Google Scholar 

  • Yadegari R, Paiva G, Laux T, Koltunow A, Apuya N, Zimmerman J, Fischer R, Harada J, Goldberg R (1994) Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6:1713–1729

    Google Scholar 

  • Zupkó I, Réthy B, Hohmann J, Molnár J, Ocsovszki I, Falkay G (2009) Antitumor activity of alkaloids derived from Amaryllidaceae species. In Vivo 23:41–48

    PubMed  Google Scholar 

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (31170225; 31201145), Major State Basic Research Development Program of China (973 Program) (2012CB026105), the National High Technology Research and Development Program (2007AA021401), Foundation of Science and Technology Program of Gansu Province (1107RJYA005), Fundamental Research Funds for the Central Universities (lzujbky-2013-bt05), Scientific research project of Qinghai-Tibetan DC Interconnection Project in State Grid Corporation of China, and the Foundation of Science and Technology Program of Gansu Province (1208RJZA224).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. State Key Laboratory of Applied Organic Chemistry and College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou, 730000, People’s Republic of China

    Yanfeng Hu & Xiaoping Cao

  2. School of Life Sciences, Lanzhou University, Lanzhou, 730000, People’s Republic of China

    Yanfeng Hu, Jiaolong Li, Lijing Yang, Wenbin Nan & Yurong Bi

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  1. Yanfeng Hu
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Correspondence to Yurong Bi.

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Handling Editor: Liwen Jiang

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Hu, Y., Li, J., Yang, L. et al. Inhibition of root growth by narciclasine is caused by DNA damage-induced cell cycle arrest in lettuce seedlings. Protoplasma 251, 1113–1124 (2014). https://doi.org/10.1007/s00709-014-0619-y

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  • DOI: https://doi.org/10.1007/s00709-014-0619-y

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