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Regulation of Cell Division and Growth in Roots of Lactuca sativa L. Seedlings by the Ent-Kaurene Diterpenoid Rabdosin B

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Abstract

Rabdosin B, an ent-kaurene diterpenoid purified from the air-dried aerial parts of Isodon japonica (Burm.f) Hara var. galaucocalyx (maxin) Hara, showed a biphasic, dose-dependent effect on root growth and a strong inhibitory effect on root hair development in lettuce seedlings (Lactuca sativa L.). Lower concentrations of rabdosin B (20–80 μM) significantly promoted root growth, but its higher levels at 120–200 μM, by contrast, had inhibitory effects. Additionally, all tested concentrations (10–40 μM) inhibited root hair development of seedlings in a dose-dependent manner. Further investigations on the underlying mechanism revealed that the promotion effect of rabdosin B at the lower concentrations resulted from increasing the cell length in the mature region and enhancing the mitotic activity of meristematic cells in seedlings’ root tips. In contrast, rabdosin B at higher concentrations inhibited root growth by affecting both cell length in the mature region and division of meristematic cells. Comet assay and cell cycle analysis demonstrated that the decrease of mitotic activity of root meristematic cells was due to DNA damage induced cell cycle retardation of the G2 phase and S phase at different times.

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References

  • Akinboro, A. and Bakare, A. A. 2007. Cytotoxic and genotoxic effects of aqueous extracts of five medicinal plants on Allium cepa Linn. J. Ethnopharmacol. 112:470–475.

    Article  CAS  PubMed  Google Scholar 

  • Angelis, K. J., Dusinska, M., and Collins, A. R. 1999. Single cell gel electrophoresis: detection of DNA damage at different levels of sensitivity. Electrophoresis 20:2133–2138.

    Article  CAS  PubMed  Google Scholar 

  • An, M., Johnson, I. R., Lovett, J. V. 1993. Mathematical modeling of allelopathy: biological response to allelochemicals and its interpretations. J. Chem. Ecol. 19:2379–2388.

    Article  CAS  Google Scholar 

  • Belz, R. G. 2008. Stimulation versus inhibition-bioactivity of parthenin, a phytochemical from Parthenium hysterophorus L. Dose-Response. 6:80–96.

    Article  CAS  Google Scholar 

  • Belz, R. G., Duke, S. O., Hurle, K. 2005. Dose-response—a challenge for allelopathy? Nonlinearity Biol. Toxicol Med. 3:173–211.

    Article  CAS  PubMed  Google Scholar 

  • Belz, R. G., Velini, E. D., and Duke, S. O. 2007. Dose/response relationships in allelopathy research, pp. 3–29, in Y. Fujii and S. Hiradate (eds.). Allelopathy. New Concepts and Methodology, Science Publishers, New Hampshire, USA.

    Google Scholar 

  • Bertin, C., Yang, X. H., and Weston, L. A. 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil. 256:67–83.

    Article  CAS  Google Scholar 

  • Blanco Fernández, A., Sánchez-Moreiras, A. M., and Coba De La Peña, T. 2001. Flow cytometry: principles and instrumentation, pp. 21–34, in M. J. Reigosa (eds.). Handbook of Plant Ecophysiology Techniques. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Burssens, S., Himanen, K., Van De Cotte, B., Beeckman, T., Van Montagu, M., Inze, D., and Verbruggen, N. 2000. Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640.

    Article  CAS  PubMed  Google Scholar 

  • Calera, M. R., Soto, F., Sanchez, P., Bye, R., Hernandez-Bautista, B., Anaya, A. L., Lotina-Hennsen, B., and Mata, R. 1995. Biochemically active sesquiterpene lactones from Ratibida mexicana. Phytochemistry 40:419–425.

    Article  CAS  PubMed  Google Scholar 

  • Cangiano, T., Dellagreca, M., Fiorentino, A., Isidori, M., Monaco, P., and Zarrelli, A. 2002. Effect of ent-labdane diterpenes from Potamogetonaceae on Selenastrum capricornutum and other aquatic organisms. J. Chem. Ecol. 28:1103–1114.

    Article  Google Scholar 

  • Cantrell, C. L., Duke, S. O., Fronczek, F. R., Osbrink, W. L. A., Mamonov, L. K., Vassilyev, J. I., Wedge, D. E., and Dayan, F. E. 2007. Phytotoxic eremophilanes from Ligularia macrophylla. J. Agric. Food Chem. 55:10656–10663.

    Article  CAS  PubMed  Google Scholar 

  • Coba De La Peña, T., and Sánchez-Moreiras, A. M. 2001. Flow cytometry: cell cycle, pp. 65–80, in M. J. Reigosa (eds.). Handbook of Plant Ecophysiology Techniques. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

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

    Google Scholar 

  • Dellagreca, M., Fiorentino, A., and Isidori, M. 2004. Bioactive compounds from Potamogetonaceae on aquatic organisms, pp. 35–56, in F. A. Macías, J. C. G. Galindo, J. M. G. Molinillo, and H. G. Cutler (eds). Allelopathy. Chemistry and Mode of Action of Allelochemicals. CRC Press, Boca Raton.

    Google Scholar 

  • Den Boer, B. G. W. and Murray, J. A. H. 2000. Triggering the cell cycle in plants. Trends Cell Biol. 10:245–250.

    Article  CAS  PubMed  Google Scholar 

  • De Veylder, L., Beeckman, T., and Inze, D. 2007. The ins and outs of the plant cell cycle. Nat. Rev. Mol. Cell Biol. 8:655–665.

    Article  CAS  PubMed  Google Scholar 

  • Ding, L., Qi, L. L., Jing, H. W., Li, J., Wang, W., and 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 

  • Dolan, L. 2001. The role of ethylene in root hair growth in Arabidopsis. J. Plant Nutr. Soil Sci. 164:141–145.

    Article  CAS  Google Scholar 

  • Dolezěl, J., Cihalikova, J., Weiserova, J., and Lucretti, S. 1999. Cell cycle synchronization in plant root meristems. Meth. Cell Sci. 21:95–107.

    Article  Google Scholar 

  • Dugardeyn, J. and Van Der Straeten, D. 2008. Ethylene: Fine-tuning plant growth and development by stimulation and inhibition of elongation. Plant Sci. 02, 003.

  • Duke, S. O. and Oliva, A. 2002. Mode of action of phytotoxic terpenoids, pp. 201–216, in F. A. Macías, J. C. G. Galindo, J. M. G. Molinillo, and H. G. Cutler (eds.). Allelopathy. Chemistry and Mode of Action of Allelochemicals. CRC Press, Boca Raton.

    Google Scholar 

  • Forde, B. and Lorenzo, H. 2001. The nutritional control of root development. Plant and Soil. 232:51–68.

    Article  CAS  Google Scholar 

  • Gichner, T., and Plewa, M. J. 1998. Induction of somatic DNA damage as measured by single cell gel electrophoresis and point mutation in leaves of tobacco plants. Mutat. Res. 401:143–152.

    CAS  PubMed  Google Scholar 

  • Gichner, T., Patková, Z., Száková, J., and Demnerová, K. 2004. Cadmium induces DNA damage in tobacco roots, but no DNA damage, somatic mutations or homologous recombination in tobacco leaves. Mutation Research. 559:49–57.

    CAS  PubMed  Google Scholar 

  • Gichner, T., Patková, Z., Száková, J., Žnidar, I., and 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 

  • Hefner, E., Huefner, N., and Britt, A. B. 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 and Dakshini, K. M. M. 1995. Allelopathic potential of an annual weed, Polygonum monspeliensis, in crops in India. Plant Soil. 173:251–257.

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

    PubMed  Google Scholar 

  • Liu, W., Yang, Y. S., Li, P., Zhou, Q., and 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 

  • Liu, G. A., Ding, L., Yang, Y., Yang, H., Yang, Q. M., and Wang, H. Q. 2006. Anti-oxidative action of ent-kaurene diterpenoids. Res. Chem. Intermed. 32:787–794.

    Article  CAS  Google Scholar 

  • Macías, F. A., Molinillo, J. M. G., Galindo, J. C. G., Varela, R. M., Torres, A., and Simonet, A. M. 1999. Terpenoids with potential use as natural herbicide templates, pp. 15–31, in H. G. Cutler and S. J. Cutler (eds.). Biologically Active Natural Products. Agrochemicals CRC, Boca Raton.

    Google Scholar 

  • Macías, F. A., Varela, R. M., Simonet, A. M., Cutler, H. G., Culter, S. J., Ross, S. A., Dunbar, D. C., Dugan, F. M., and Hill, R. A. 2000. (+)-Brevione A. The first member of a novel family of bioactive spiroditerpenoids isolated from Penicillium brevicompactum Dierckx. Tetrahedron Lett. 41:2683–2686.

    Article  Google Scholar 

  • Macías, F. A., Torres, A., Galindo, J. C. G., Varela, R. M., Álvarez, J. A., and Molinillo, J. M. G. 2002. Bioactive terpenoids from sunflower leaves cv. Peredovick. Phytochemistry 61:687–692.

    Article  PubMed  Google Scholar 

  • Macías, F. A., Molinillo, J. M. G., Chinchilla, D., and Galindo, J. C. G. 2004. Heliannanes-a structure-activity relationship (SAR) study, pp. 103–124, in F. A. Macías, J. C. G. Galindo, J. M. G. Molinillo, and H. G. Cutler (eds.). Allelopathy. Chemistry and mode of action of allelochemicals. CRC Press, Boca Raton.

    Google Scholar 

  • Macías, F. A., Molinillo, J. M. G., Varela, R. M., and Galindo, J. C. G. 2007. Allelopathy. A natural alternative for weed control. Pest Management Sci 63:327–348.

    Article  Google Scholar 

  • Macías, F. A., López, A., Varela, R. M., Torres, A., and Molinillo, J. M. G. 2008. Helikauranoside A, a new bioactive diterpene. J.Chem.Ecol. 34:65–69.

    Article  PubMed  Google Scholar 

  • Morales-Flores, F., Aguilar, M. I., King-Díaz, B., De Santiago-Gómez, J.-R., and Lotina-Hennsen, B. 2007. Natural diterpenes from Croton ciliatoglanduliferus as photosystem II and photosystem I inhibitors in spinach chloroplasts. Photosynth. Res. 91:71–80.

    Article  CAS  PubMed  Google Scholar 

  • Morimoto, M. and Komai, K. 2005. Plant growth inhibitors: Patchoulane-type sesquiterpenes from Cyperus rotundus L. Weed. Biol. Manag. 5:203–209.

    Article  CAS  Google Scholar 

  • Muller, C. H. 1966. The role of chemical inhibition (allelopathy) in vegetational composition. Bull. Torrey Bot. Club. 93:332–351.

    Article  CAS  Google Scholar 

  • Nishida, N., Tamotsu, S., Nagata, N., Saito, C., and Sakai, A. 2005. Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. J. Chem. Ecol. 31:1187–1203.

    Article  CAS  PubMed  Google Scholar 

  • Pan, J. W., Zhu, M. Y., and Chen, H. 2001. Aluminum-induced cell death in root-tip cells of barley. Envir. Exp. Bot. 46:71–79.

    Article  CAS  Google Scholar 

  • Parker, J. S., Cavell, A. C., Dolan, L., Roberts, K., and Grierson, C. S. 2000. Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell. 12:1961–1974.

    Article  CAS  PubMed  Google Scholar 

  • Peres, A., Churchman, M. L., Hariharan, S., Himanen, K., Verkest, A., Vandepoele, K., Magyar, Z., Hatzfeld, Y., Van Der Schueren, E., and Beemster, G. T. S. 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 

  • Reichheld, J. P., Vernoux, T., Lardon, F., Van Montagu, M., and Inzé, D. 1999. Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17, 647.

    Article  CAS  Google Scholar 

  • Reigosa, M. J. and Pazos-Malvido, E. 2007. Phytotoxic effects of 21 plant secondary metabolites on Arabidopsis thaliana germination and root growth. J. Chem. Ecol. 33:1456–1466.

    Article  CAS  PubMed  Google Scholar 

  • Rice, E. P. 1984. Allelopathy, second ed. Academic Press, London.

    Google Scholar 

  • Sánchez-Moreiras, A. M., Coba De La Peña, T., and Reigosa, M. J. 2008. The natural compound benzoxazolin-2(3H)-one selectively retards cell cycle in lettuce root meristems. Phytochemistry 05, 014.

    Google Scholar 

  • Skaltsa, H., Lazari, D., Panagouleas, C., Georgiadou, E., Garcia, B., and Sokovic, M. 2000. Sesquiterpene lactones from Centaurea thessala and Centaurea attica. Antifungal activity. Phytochemistry 55:903-908.

    Article  CAS  PubMed  Google Scholar 

  • Sun, H. D., Xu, Y. L., and Jiang, B. 2001. Diterpenoids from Isodon Species. Science, Beijing.

    Google Scholar 

  • Szabo, L. G. 2000. Juglone index: A possibility for expressing allelopathic potential of plant taxa with various life strategies. Acta Bot. Hung. 42:295–305.

    Google Scholar 

  • Tice, R. R., Agurell, E., Anderson, D., Burlinson, B., Hartmann, A., Kobayashi, H., Miyamae, Y., Rojas, E., Ryu, J. C., and Sasaki, Y. F. 2000. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen. 35:206–221.

    Article  CAS  PubMed  Google Scholar 

  • Vaccarini, E. E., Palacios, S. M., Meragelman, K. M., and Sosa, V. E. 1999. Phytogrowth-inhibitory activities of a clerodane from Viguiera tucumanensis. Phytochemistry 50:227–230.

    Article  CAS  Google Scholar 

  • West, G., Inze, D., and Beemster, G. T. S. 2004. Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol. 135:1050–1058.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yang, X., Owens, T. G., Scheffler, B. E., and Weston, L. A. 2004. Manipulation of root hair development and sorgoleone production in sorghum seedlings. J. Chem. Ecol. 30:199–213.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the National Natural Science Foundation of China (No-30960464), the Key (Key grant) Project of Chinese Ministry of Education (No-208147) and the Foundation of the Innovation Project Council of Northwest Normal University (NWNU-KJCXGC-03). Gratitude is also given to the anonymous reviewers and editors whose suggestions greatly improved our work.

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  1. College of Life Sciences, Northwest Normal University, No. 967 Anning East Road, Lanzhou, 730070, People’s Republic of China

    Lan Ding, Hongwei Jing, Linlin Qi, Jing Li, Tao Wang & Guoan Liu

  2. Key Laboratory for Natural Medicine of Gansu Province, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, Lanzhou, 730000, People’s Republic of China

    Bo Qin

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  1. Lan Ding
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  2. Hongwei Jing
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Correspondence to Lan Ding.

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Lan Ding and Hongwei Jing—co-first-authors.

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Ding, L., Jing, H., Qin, B. et al. 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 (2010). https://doi.org/10.1007/s10886-010-9783-5

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