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Plant and Soil

, Volume 327, Issue 1–2, pp 455–463 | Cite as

Effects of aqueous root extracts and hydrophobic root exudates of cucumber (Cucumis sativus L.) on nuclei DNA content and expression of cell cycle-related genes in cucumber radicles

  • Yun Zhang
  • Min Gu
  • Kai Shi
  • Yan Hong Zhou
  • Jing Quan Yu
Regular Article

Abstract

Allelopathic interactions implicate the inhibition of cell division by allelochemicals. To examine the effects of autotoxic agents on cell cycle and plant growth, germinated cucumber seeds (Cucumis sativus L.) were incubated in solutions containing the aqueous root extracts of cucumber at 1:100, 1:50, 1:25 and 1:10 (w:v), or the hydrophobic root exudates of cucumber at 25, 50 and 100 mg·L−1. Aqueous root extracts and hydrophobic root exudates inhibited radicle elongation by 36.47–60.18% and 38.24–62.50%, respectively. The mitosis-specific genes were down-regulated in roots exposed to aqueous root extracts and hydrophobic root exudates. Meanwhile, exposure to either aqueous root extracts or hydrophobic root exudates decreased the proportion of 2C (C-value) and increased the proportion of 8C, leading to an increased mean C-value. We conclude that autotoxic agent-induced inhibition of radicle growth was partly attributed to the down-regulation of cell cycle-related genes and endoreduplication was enhanced under our experimental condition.

Keywords

Allelopathy Autotoxicity Cell division Cyclins CDKs Endoreduplication 

Notes

Acknowledgement

This work was supported by the National Basic Research Program of China (2009CB11900), National Key Project of Scientific and Technical Supporting Programs of China (2008BADA6B02, 2006BAD07B03).

References

  1. Andersen SU, Buechel S, Zhao Z, Ljung K, Novák O, Busch W, Schuster C, Lohmann JU (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20:88–100CrossRefPubMedGoogle Scholar
  2. Anderson RC, Loucks OL (1966) Osmotic pressure influence in germination tests for antibiosis. Science 152:771–773CrossRefPubMedGoogle Scholar
  3. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380CrossRefPubMedGoogle Scholar
  4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefPubMedGoogle Scholar
  5. Barow M, Meister A (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ 26:571–584CrossRefGoogle Scholar
  6. Barrôco RM, Poucke KV, Bergervoet JHW, Veylder LD, Groot SPC, Inzé D, Engler G (2005) The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol 137:127–140CrossRefPubMedGoogle Scholar
  7. Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526CrossRefPubMedGoogle Scholar
  8. Beemster GTS, Vusser KD, Tavemier ED, Bock KD, Inzé D (2002) Variation in growth rate between Arabidopsis ecotypes is correlated with cell division and A-type cyclin-dependent kinase activity. Plant Physiol 129:854–864CrossRefPubMedGoogle Scholar
  9. Beemster GTS, Fiorani F, Inzé D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158CrossRefPubMedGoogle Scholar
  10. Bertin N (2005) Analysis of the tomato fruit growth response to temperature and plant fruit load in relation to cell division, cell expansion and DNA endoreduplication. Ann Bot 95:439–447CrossRefPubMedGoogle Scholar
  11. Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizophere. Plant Soil 256:67–83CrossRefGoogle Scholar
  12. Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51CrossRefPubMedGoogle Scholar
  13. Boudolf V, Vlieghe K, Beemster GTS, Magyar Z, Acosta JAT, Maes S, Schueren EVD, Inzé D, Veylder LD (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16:2683–2692CrossRefPubMedGoogle Scholar
  14. Burgos NR, Talbert RE, Kim KS, Kuk YI (2004) Growth inhibition and root ultrastructure of cucumber seedlings exposed to allelochemicals from rye (Secale cereale). J Chem Ecol 30:671–689CrossRefPubMedGoogle Scholar
  15. Burssens S, Himanen K, Cotte BV, Beeckman T, Montagu MV, Inze D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640CrossRefPubMedGoogle Scholar
  16. Callaway RM, Aschehoug ET (2000) Invasive plant versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523CrossRefPubMedGoogle Scholar
  17. Chon SU, Choi SK, Jung S, Jang HG, Pyo BS, Kim SM (2002) Effects of alfalfa leaf extracts and phenolic allelochemicals on early seedling growth and root morphology of alfalfa and barnyard grass. Crop Prot 21:1077–1082CrossRefGoogle Scholar
  18. Cruz-Ortega R, Ayala-Cordero G, Anaya AL (2002) Allelochemical stress produced by the aqueous leachate of Callicarpa acuminate: effects on roots of bean, maize and tomato. Physiol Plant 116:20–27CrossRefPubMedGoogle Scholar
  19. Den Boer BGW, Murray JAH (2000) Control of plant growth and development through manipulation of cell cycle genes. Curr Opin Biotech 11:138–145CrossRefGoogle Scholar
  20. Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264CrossRefPubMedGoogle Scholar
  21. Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J Exp Bot 58:3765–3773CrossRefPubMedGoogle Scholar
  22. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419CrossRefPubMedGoogle Scholar
  23. Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105:297–306CrossRefPubMedGoogle Scholar
  24. Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7CrossRefGoogle Scholar
  25. Flores HE, Vivanco JM, Loyola-Vargas VM (1999) “Radicle” biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226CrossRefPubMedGoogle Scholar
  26. Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051CrossRefPubMedGoogle Scholar
  27. Gilissen LJ, van Staveren MJ, Creemers-Molenaar J, Verhoeven HA (1993) Development of polysomaty in seedlings and plants of Cucumis sativus L. Plant Sci 91:171–179CrossRefGoogle Scholar
  28. Granier C, Inzé D, Tardieu F (2000) Spatial distribution of cell division rate can be deduced from that of p34cdc2 kinase activity in maize leaves grown at contrasting temperature and soil water conditions. Plant Physiol 124:1392–1402CrossRefGoogle Scholar
  29. Greilhuber J (2008) Cytochemistry and C-values: The less-well-known world of nuclear DNA amounts. Ann Bot 101:791–804CrossRefPubMedGoogle Scholar
  30. Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot 95:255–260CrossRefPubMedGoogle Scholar
  31. Hemerly A, Bergounioux C, van Montagu M, Inzé D, Ferreira P (1992) Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc Natl Acad Sci USA 1589:3295–3299CrossRefGoogle Scholar
  32. Inderjit, Callaway RM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11CrossRefGoogle Scholar
  33. Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annual Review in Genet 40:77–105CrossRefGoogle Scholar
  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2T−ΔΔC method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  35. Menges M, Samland AK, Planchais S, Murray JAH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906CrossRefPubMedGoogle Scholar
  36. Mironov V, de Veylder L, Van M, Inzé D (1999) Cyclin-dependent kinases and cell division in plants- the nexus. Plant Cell 11:509–522CrossRefPubMedGoogle Scholar
  37. Nishida N, Tamotsu S, Nagata N, Saito C, 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 31:1187–1203CrossRefPubMedGoogle Scholar
  38. Pines J (1995) Cyclins and cyclin-dependent kinases: a biochemical view. Biochem J 388:697–711Google Scholar
  39. Putnam AR (1985) Allelopathic research in agriculture: past highlights and potential. In: Thompson AC (ed) The chemistry of allelopathy: biochemical interactions among plants. American Chemical Society, Washington, pp 1–8CrossRefGoogle Scholar
  40. Repetto O, Massa N, Gianinazzi-Pearson V, Dumas-Gaudot E, Berta G (2007) Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 17:111–120CrossRefPubMedGoogle Scholar
  41. Rice EL (1984) Allelopathy, 2nd edn. Academic, New YorkGoogle Scholar
  42. Rosiak M, Polit J, Maszewski J (2002) Staurosporine and vanadate can induce additional endo-S phases during cell differentiation in primary root of Pisum sativum. Plant Sci 163:889–895CrossRefGoogle Scholar
  43. Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438CrossRefPubMedGoogle Scholar
  44. Sánchez-Moreiras AM, De La Peña TC, Reigosa MJ (2008) The natural compound benzoxazolin-2(3H)-one selectively retards cell cycle in lettuce root meristems. Phytochemistry 69:2172–2179CrossRefPubMedGoogle Scholar
  45. Schuppler U, He PH, John PCL, Munns R (1998) Effect of water stress on cell division and cell-division-cycle 2-like cell-cycle kinase activity in wheat leaves. Plant Physiol 117:667–678CrossRefPubMedGoogle Scholar
  46. Setter TL, Flannigan BA (2001) Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J Exp Bot 52:1401–1408CrossRefPubMedGoogle Scholar
  47. Singh HP, Batish DR, Kohli RK (1999) Autotoxicity: concept, organisms, and ecological significance. Crit Rev Plant Sci 18:757–772CrossRefGoogle Scholar
  48. Tang CS, Young CC (1982) Collection and identification of allelopathic compounds from the undisturbed root system of Bigalta Limpograss (Hemarthria altissima). Plant Physiol 69:155–160CrossRefPubMedGoogle Scholar
  49. Uren NC (2000) Types, amounts and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc, New York, pp 19–40Google Scholar
  50. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51CrossRefPubMedGoogle Scholar
  51. Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479CrossRefPubMedGoogle Scholar
  52. West G, Inzé D, Beemster GTS (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058CrossRefPubMedGoogle Scholar
  53. Wu HW, Pratley J, Lemerle D, An M, Liu DL (2007) Autotoxicity of wheat (Triticum aestivum L.) as determined by laboratory bioassays. Plant Soil 296:85–93CrossRefGoogle Scholar
  54. Ye SF, Yu JQ, Peng YH, Zheng JH, Zou LY (2004) Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263:143–150CrossRefGoogle Scholar
  55. Ye SF, Zhou YH, Sun Y, Zou LY, Yu JQ (2006) Cinnamic acid causes oxidative stress in cucumber roots and promotes incidence of Fusarium wilt. Environ Exp Bot 56:255–262CrossRefGoogle Scholar
  56. Young CC (1984) Autotoxication in root exudates of Asparagus officinalis L. Plant Soil 82:247–253CrossRefGoogle Scholar
  57. Yu JQ, Matsui Y (1994) Phytotoxic substances in the root exudates of Cucumis sativus L. J Chem Ecol 20:21–31CrossRefGoogle Scholar
  58. Yu JQ, Shou SY, Qian YR, Hu WH (2000) Autotoxic potential in cucurbit crops. Plant Soil 223:147–151CrossRefGoogle Scholar
  59. Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates, aqueous root extracts of cucumber (Cucumis sativus L.) and allelochemicals on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Yun Zhang
    • 1
  • Min Gu
    • 1
  • Kai Shi
    • 1
  • Yan Hong Zhou
    • 1
  • Jing Quan Yu
    • 1
    • 2
  1. 1.Department of Horticulture, Huajiachi CampusZhejiang UniversityHangzhouP.R. China
  2. 2.Key Laboratory of Horticultural Plants Growth, Development and Biotechnology, Agricultural Ministry of ChinaHangzhouP.R. China

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