Abstract
The involvement of gibberellins in 1,8-cineole-mediated inhibition of tuber sprout growth was investigated in non-dormant field- and greenhouse-grown tubers of Russet Burbank. Continuous exposure of tubers to cineole in the vapor-phase resulted in a dose-dependent inhibition of sprout growth. Comparative studies using plant bioassay systems whose growth was differentially dependent on cell division, cell elongation, or both demonstrated that cineole had no direct effect on either process. Of the assays used, only cineole-mediated inhibition of etiolated hypocotyl growth mirrored the inhibition of tuber sprout growth which suggested an effect on gibberellin synthesis or action. Both GA19 and GA20 were detected in extracts prepared from control sprouts but only GA19 was found in extracts prepared from cineole treated sprouts. Exogenous GA3, GA20, and GA1 (but not GA19) reversed cineole-mediated sprout growth inhibition. Expression of genes encoding key GA metabolic enzymes was altered by cineole treatment in a manner consistent with diminished endogenous GA content. Collectively, these results suggest that the inhibition of sprout growth by low vapor-phase concentrations of cineole is in part a result of impaired GA biosynthesis resulting in a reduction in bioactive GA content.
Resumen
Se investigó el involucramiento de giberelinas en la inhibición del crecimiento del brote de tubérculo mediado por 1,8-cineole, en tubérculos en dormancia del campo y del invernadero de Russet Burbank. La exposición continua de los tubérculos a cineole en la fase de vapor dio por resultado una inhibición del crecimiento del brote dependiente de la dosis. Estudios comparativos usando sistemas de bioensayos de plantas cuyo crecimiento era diferencialmente dependiente de la división celular, elongación celular, o ambas, demostraron que cineole no tuvo efecto directo en ninguno de los procesos. De los ensayos usados, solamente la inhibición mediada por cineole de crecimiento de hipocotilo elongado, reflejó la inhibición del crecimiento del brote de tubérculo, lo cual sugirió un efecto en la síntesis o acción de giberelina. Se detectaron GA19 y GA20 en extractos preparados de los brotes testigo, pero solo el GA19 se encontró en los extractos de brotes tratados con cineole. La aplicación exógena de GA3, GA20 y GA1 (no GA 19) revirtió la inhibición del crecimiento del brote mediada por cineole. Se alteró la expresión de los genes que codifican las enzimas metabólicas clave de GA mediante el tratamiento con cineole de manera consistente con la disminución del contenido endógeno de GA. Colectivamente, estos resultados sugieren que la inhibición del crecimiento del brote por bajas concentraciones de cineole en fase de vapor es en parte un resultado de la biosíntesis debilitada de GA, resultando en una reducción del contenido de GA bioactivo.
Similar content being viewed by others
Abbreviations
- (DMSO):
-
Dimethyl sulfoxide
- (GA):
-
Gibberellin
- (MS):
-
Murashige Skoog
- (PCR):
-
Polymerase Chain Reaction
- (UPLC ESI-MS/MS):
-
ultra-high-performance liquid chromatography-electrospray ionization tandem mass spectrometry
References
Baydar, H., and T. Karadogan. 2004. The effects of volatile oils on in vitro potato sprout growth. Potato Research 46: 1–8.
Brown, R.G.S., H. Kawaide, Y. Yang, W. Rademacher, and Y. Kamiya. 1997. Daminozide and prohexadione have similar modes of action as inhibitors of the late stages of gibberellin metabolism. Physiologia Plantarum 101: 309–313.
Burton, W.G. 1989. The Potato 3rd Edition, 470–504. Essex: Longman Scientific & Technical.
Burton, W.G., and D.F. Meigh. 1971. The production of growth-suppressing volatile substances by stored potato tubers. Potato Research 14: 96–101.
Campbell, M.A., A. Gleichsner, L. Hilldorfer, D. Horvath, and J. Suttle. 2012. The sprout inhibitor 1,4-dimethylnaphthalene induces the expression of the cell cycle inhibitors KRP1 and KRP2 in potatoes. Functional and Integrative Genomics 12: 533–541.
Chiwocha, S.D.S., S.R. Abrams, S.J. Ambrose, A.J. Cutler, M. Loewen, A.R.S. Ross, and A.R. Kermode. 2003. A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant Journal 3: 405–417.
Coleman, W.K., D.J. Donnelly, and S.E. Coleman. 2001. Potato microtubers as research tools: a review. American Journal of Potato Research 78: 47–55.
Crowell, P.L., Z. Ren, S. Lin, E. Vedejs, and M.N. Gould. 1994. Structure-activity relationships among monoterpene inhibitors of protein isoprenylation and cell proliferation. Biochemical Pharmacology 47: 1405–1415.
Franklin, B., and P.F. Wareing. 1960. Effect of gibberellic acid on hypocotyl growth of lettuce seedlings. Nature 185: 255–256.
Jones, M.G., R. Horgan, and M.A. Hall. 1988. Endogenous gibberellins in the potato (Solanum tuberosum). Phytochemistry 27: 7–10.
Kawai, Y., E. Ono, and M. Mizutani. 2014. Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant Journal 78: 328–343.
Kleinkopf, G.E., N.A. Oberg, and N.L. Olsen. 2003. Sprout inhibition in storage: current status, new chemistries and natural compounds. American Journal of Potato Research 80: 317–327.
Knowles, L.O., and N.R. Knowles. 2012. Toxicity and metabolism of exogenous α, ß-unsaturated carbonyls in potato (Solanum tuberosum L.) tubers. Journal of Agricultural and Food Chemistry 60: 11173–11181.
Meigh, D.F. 1969. Suppression of sprouting in stored potatoes by volatile organic compounds. Journal of the Science of Food and Agriculture 20: 160–164.
Meigh, D.F., A. Authur, E. Filmer, and R. Self. 1973. Growth-inhibitory volatile aromatic compounds produced by Solanum tuberosum tubers. Phytochemistry 12: 987–993.
Moreland, D.E. 1980. Mechanisms of action of herbicides. Annual Review of Plant Physiology 31: 597–638.
Muller, C.H., W.H. Muller, and B.L. Haines. 1964. Volatile growth inhibitors produced by aromatic shrubs. Science 143: 471–473.
Nakayama, I., M. Kobayashi, Y. Kamiya, H. Abe, and A. Sakuai. 1992. Effects of a plant-growth regulator, prohexadione-calcium (BX-112), on the endogenous levels of gibberellins in rice. Plant & Cell Physiology 33: 59–62.
Rademacher, W. 2000. Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology 51: 501–532.
Romagni, J.G., S.N. Allen, and F.E. Dayan. 2000. Allelopathic effects of volatile cineoles on two weedy plant species. Journal of Chemical Ecology 26: 303–313.
Sikkema J, JAM deBont, and B Poolman. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews 59:201–222.
Sĭmko, I. 1994. Effect of paclobutrazol on in vitro formation of microtubers and their sprouting after storage. Biologia Plantarum 36: 15–20.
Sponsel, V.M., and P. Heddon. 2004. Gibberellin biosynthesis and inactivation. In In plant hormones: biosynthesis, signal transduction, action! ed. P.J. Davies, 63–94. Dordrecht: Kluwer.
Suttle, J.C. 2004. Involvement of endogenous gibberellins in potato tuber dormancy and early sprout growth: a critical assessment. Journal of Plant Physiology 161: 157–164.
Suttle, J.C., L.L. Huckle, S. Lu, and D.C. Knauber. 2014. Potato tuber cytokinin oxidase/dehydrogenase genes: biochemical properties, activity, and expression during tuber dormancy progression. Journal of Plant Physiology 171: 448–457.
Suttle JC, MA Campbell, and NL Olsen. 2015. Potato tuber dormancy and postharvest sprout control. In: Postharvest Ripening Physiology in Crops. Ed. S. Pareek. CRC Press, Boca Raton. In Press.
Teper-Bamnolker, P., N. Dudai, R. Fischer, E. Belausov, H. Zemach, O. Shoseyov, and D. Eshel. 2010. Mint essential oil can induce or inhibit potato sprouting by differential alteration of apical meristem. Planta 232: 179–186.
Tsai, C.-J., S.A. Harding, T.J. Tschaplinski, R.L. Lindroth, and Y. Yuan. 2006. Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytologist 172: 47–62.
Vaughn, S.F., and G.F. Spencer. 1991. Volatile monoterpenes inhibit potato tuber sprouting. American Journal of Potato Research 68: 821–831.
Vaughn, S.F., and G.F. Spencer. 1993. Volatile monoterpenes as potential parent structures for new herbicides. Weed Science 41: 114–119.
Yamaguchi, S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59: 225–251.
Yu, V., S. Rakitin, V. Vladimirtseva, and L.N. Nikolaeva. 1978. Action of maleic hydrazide on RNA and protein synthesis in growing potato buds. Fiziologiya Rastenii 25: 223–229.
Author information
Authors and Affiliations
Corresponding author
Additional information
Mention of company or trademark does not imply endorsement by the United States Department of Agriculture over others not named.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplemental Table 1
(DOCX 13 kb)
Rights and permissions
About this article
Cite this article
Suttle, J.C., Olson, L.L. & Lulai, E.C. The Involvement of Gibberellins in 1,8-Cineole-Mediated Inhibition of Sprout Growth in Russet Burbank Tubers. Am. J. Potato Res. 93, 72–79 (2016). https://doi.org/10.1007/s12230-015-9490-4
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12230-015-9490-4