Skip to main content
Log in

The Effects of Dormancy Status on the Endogenous Contents and Biological Activities of Jasmonic Acid, N-(jasmonoyl)-Isoleucine, and Tuberonic Acid in Potato Tubers

  • Published:
American Journal of Potato Research Aims and scope Submit manuscript

Abstract

The effects of storage and dormancy progression on the endogenous contents and the growth-regulating activities of jasmonic acid (JA), jasmonoyl-isoleucine (JA-Ile), and tuberonic acid (TA) were determined in potato (Solanum tuberosum L. cv. Russet Burbank) minitubers and seed tubers over several harvest/storage seasons. In apical discs (consisting of both periderm and buds) isolated from minitubers undergoing natural dormancy progression, JA content was low immediately after harvest, remained essentially constant as dormancy weakened, rose >4-fold as sprouting commenced and declined by >50% as sprouting became more vigorous. JA-Ile content was more variable; remaining constant over 7 months of storage in 1 year and increasing ca. 5-fold over the same period during a second year. The TA content of minituber apical discs exceeded that of JA or JA-Ile by >20-fold and declined steadily to ca. 50% of initial levels during storage and dormancy progression. A similar but more temporally compressed pattern was found in chemically forced minituber apical discs following a 24 h treatment with the synthetic dormancy terminating agent bromoethane. A different pattern was observed in meristems isolated from seed tubers at three stages of dormancy progression. JA content was low in dormant meristems and remained constant in meristems isolated at late dormancy and following dormancy exit. The content of JA-Ile rose gradually as meristems progressed from deep dormancy to active sprouting. The TA content of isolated meristems was >20-fold higher than either JA or JA-Ile and rose slightly during dormancy progression. Exogenous JA (0.001 to 1 mM) had no effect on sprout growth when applied to intact non-dormant minitubers but treatment with 1 mM JA-Ile inhibited sprout growth by 35%. In contrast, direct application of 10 μg JA to single-eye tissue cylinders resulted in a 29% inhibition of sprout growth after 2 weeks while JA-Ile had no effect. Treatment of dormant minitubers with either JA or JA-Ile (0.01to1 mM) had no effect on dormancy duration or subsequent sprout growth. Collectively, these data do not support a major role for JA or its metabolites JA-Ile and TA in potato tuber dormancy control but they do not exclude other roles for these hormones in tuber physiology and early sprout growth.

Resumen

En minitubérculos y en tubérculos-semilla de papa (Solanum tuberosum L. cv. Russet Burbank) se determinaron durante varias temporadas de cosecha/almacenaje, los efectos del almacenamiento y del avance de la dormancia en el contenido endógeno y en actividades reguladoras del crecimiento del ácido jasmónico (JA), jasmonoyl-isoleucina (JA-Ile) y ácido tuberónico (TA). En discos apicales (consistentes en tanto peridermo como yemas) aislados de minitubérculos en pleno avance de dormancia natural, el contenido de JA fue bajo inmediatamente después de la cosecha, permaneciendo esencialmente constante a medida que la dormancia se debilitaba, aumentando más de cuatro veces su contenido cuando empezó la brotación y declinó a más del 50% a medida que la brotación se hizo más vigorosa. El contenido de JA-Ile fue más variable; permaneciendo constante durante siete meses de almacenamiento en un año y aumentando aproximadamente cinco veces sobre el mismo período durante el segundo año. El contenido de TA en discos apicales de minitubérculo excedió al de JA o JA-Ile por mas de 20 veces y declinó establemente a aproximadamente 50% de los niveles iniciales durante el progreso del almacenamiento y la dormancia. Se encontró un patrón similar pero mas temporalmente compacto en discos apicales de minitubérculos químicamente forzados después de 24 hs de tratamiento con el agente rompedor de dormancia bromoethano. Se observó un patrón diferente en meristemos aislados de tubérculos-semilla en tres estados de avance de la dormancia. El contenido de JA fue bajo en meristemos en dormancia y permaneció constante en meristemos aislados en dormancia tardía y después de la salida de la dormancia. El contenido de JA-Ile aumentó gradualmente a medida que los meristemos avanzaron de dormancia profunda a brotación activa. El contenido de TA de meristemos aislados fue 20 veces más alto que tanto JA o JA-Ile y aumentó ligeramente durante el avance de la dormancia. JA exógeno (0.001 a 1 mM) no tuvo efecto en el crecimiento del brote cuando se aplicó a minitubérculos intactos no en dormancia, pero tratamientos con 1 mM de JA-Ile inhibió el crecimiento del brote en un 35%. En contraste, la aplicación directa de 10 μg de JA a cilindros de tejido de un ojo individual resultó en un 29% de inhibición del crecimiento del brote después de dos semanas, mientras que JA-Ile no tuvo efecto. El tratamiento de minitubérculos en dormancia, ya fuera con JA o JA-Ile (0.01 a 1 mM) no tuvo efectos en la duración de la dormancia o en el crecimiento subsecuente del brote. Colectivamente, estos datos no respaldan un papel importante para JA o sus metabolitos JA-Ile y TA en el control de la dormancia de tubérculos de papa, pero no excluyen otros papeles para estas hormonas en la fisiología del tubérculo y en el crecimiento temprano del brote.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

BE:

Bromoethane

DJA:

Dihydrojasmonic acid

GC-MS:

Gas-liquid chromatography/mass spectrometry

JA:

Jasmonic acid

LC-MS-SIM:

Liquid chromatography-mass spectrometry-single-ion monitoring

JA-Ile:

N-(jasmonoyl)-L-isoleucine

TA:

Tuberonic acid

References

  • Abdala, G., G. Castro, O. Miersch, and D. Pearce. 2002. Changes in jasmonate and gibberellin levels during development of potato plants. Plant Growth Regulation 36: 121–126.

    Article  CAS  Google Scholar 

  • Bachem, C., R. van der Hoeven, J. Lucker, R. Oomen, E. Casarini, E. Jacobsen, and R. Visser. 2000. Functional genomic analysis of potato tuber life-cycle. Potato Research 43: 297–312.

    Article  CAS  Google Scholar 

  • Bazabakana, R., J.-L. Fauconnier, B. Diallo, J.P. Dupont, J. Homes, and M. Jaziri. 1999. Control of Dioscorea alata microtuber dormancy and germination by jasmonic acid. Plant Growth Regulation 27: 113–117.

    Article  CAS  Google Scholar 

  • Browse, J. 2009. Jasmonate passes muster: a receptor and targets for the defense hormone. Annual Review of Plant Biology 60: 183–205.

    Article  PubMed  CAS  Google Scholar 

  • Burton, W.G. 1989. The potato, 3rd ed, 470–504. Essex: Longman Scientific and Technical.

    Google Scholar 

  • Campbell, M.A., E. Segear, L. Beers, D. Knauber, and J. Suttle. 2008. Dormancy in potato tuber meristems: chemically induced cessation in dormancy matches the natural process based on transcript profiles. Functional & Integrative Genomics 8: 317–328.

    Article  CAS  Google Scholar 

  • Castro, G., T. Kraus, and G. Abdala. 1999. Endogenous jasmonic acid and radial cell expansion in buds of potato tubers. Journal of Plant Physiology 155: 706–710.

    CAS  Google Scholar 

  • Cenzano, A., A. Vigliocco, O. Miersch, and G. Abdala. 2005. Hydroxylated jamonate levels during stolon to tuber transition in Solanum tuberosum L. Potato Research 48: 107–115.

    Article  Google Scholar 

  • Claassens, M.M.J., and D. Vreugdenhil. 2000. Is dormancy breaking of potato tubers the reverse of tuber initiation? Potato Research 43: 347–369.

    Article  CAS  Google Scholar 

  • Coleman, W.K. 1983. An evaluation of bromoethane for breaking tuber dormancy in Solanum tuberosum L. American Potato Journal 60: 161–167.

    Article  CAS  Google Scholar 

  • Coleman, W.K. 2000. Physiological aging of potato tubers: a review. The Annals of Applied Biology 137: 189–199.

    Article  Google Scholar 

  • Corbineau, F., R.M. Rudnicki, and D. Come. 1988. The effects of methyl jasmonate on sunflower (Helianthus annuus L.) seed germination and seedling development. Plant Growth Regulation 7: 157–169.

    CAS  Google Scholar 

  • Désiré, S., J.-P. Couillerot, J.-L. Hilbert, and J. Vasseur. 1995. Protein changes in Solanum tuberosum during storage and dormancy breaking of in vitro microtubers. Plant Physiology and Biochemistry 33: 479–487.

    Google Scholar 

  • Destefano-Beltrán, L., D. Knauber, L. Huckle, and J. Suttle. 2006. Chemically forced dormancy termination mimics natural dormancy progression in potato tuber meristems by reducing ABA content and modifying expression of gene involved in regulating ABA synthesis and metabolism. Journal of Experimental Botany 57: 2879–2886.

    Article  PubMed  Google Scholar 

  • Donnelly, D.J., W.K. Coleman, and S.E. Coleman. 2003. Potato microtuber production and performance: a review. American Journal of Potato Research 80: 103–115.

    Article  Google Scholar 

  • Eschen-Lippold, L., S. Altmann, C. Gebhart, C. Göbel, I. Feussner, and S. Rosahl. 2010. Oxylipins are not required for R gene-mediated resistance in potato. European Journal of Plant Pathology 127: 437–442.

    Article  CAS  Google Scholar 

  • Fonseca, S., A. Chini, M. Hamberg, B. Adie, A. Porzel, R. Kramell, O. Miersch, C. Waternack, and R. Solano. 2009. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344–350.

    Article  PubMed  CAS  Google Scholar 

  • Gregory, L.E. 1956. Some factors for tuberization in the potato plant. American Journal of Botany 43: 281–288.

    Article  CAS  Google Scholar 

  • Hannapel, D.J. 2007. Signalling the induction of tuber formation. In Potato biology and biotechnology: Advances and perspectives, ed. D. Vreugdenhil, J. Bradshaw, C. Gebhart, F. Govers, M.A. Taylor, D.K.L. MacKerron, and H.A. Ross, 237–256. Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Harms, K., R. Atzorn, A. Brash, H. Kűhn, C. Wasternack, L. Willmitzer, and H. Peña-Cortes. 1995. Expression of a flax allene oxide synthase cDNA leads to increased endogenous jasmonic acid levels in transgenic potato plants but not to a corresponding activation of JA-responding genes. The Plant Cell 7: 1645–1654.

    Article  PubMed  CAS  Google Scholar 

  • Haverkort, A.J. 2007. Potato crop response to radiation and daylength. In Potato biology and biotechnology: Advances and perspectives, ed. D. Vreugdenhil, J. Bradshaw, C. Gebhart, F. Govers, M.A. Taylor, D.K.L. MacKerron, and H.A. Ross, 237–256. Amsterdam: Elsevier.

    Google Scholar 

  • Helder, H., O. Miersch, K. Vreugdenhil, and G. Sembdner. 1993. Occurrence of hydroxylated jasmonic acids in leaflets of Solanum demissum plants grown under long- and short-day conditions. Physiologia Plantarum 88: 647–653.

    Article  CAS  Google Scholar 

  • Jásik, J., and G.-J. de Klerk. 2006. Effect of methyl jasmonate on morphology and dormancy development in lily bulbets regenerated in vitro. Journal of Plant Growth Regulation 25: 45–51.

    Article  Google Scholar 

  • Jikamaru, Y., T. Asami, H. Seto, S. Yoshida, T. Yokoyama, N. Obara, M. Hasegawa, O. Kodama, M. Nishiyama, K. Okada, H. Nojiri, and H. Yamane. 2004. Preparation and biological activity of molecular probes to identify and analyze jasmonic acid-binding proteins. Bioscience, Biotechnology, and Biochemistry 68: 1461–1468.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Krammel, R., J. Schmidt, G. Schneider, G. Sembdner, and K. Schreiber. 1988. Synthesis of N-(jasmonoyl)amino acid conjugates. Tetrahedron 44: 5791–5807.

    Article  Google Scholar 

  • Lulai, E.C., P.H. Orr, and M.T. Glynn. 1995. US Patent 5436226.

  • Lulai, E., L. Huckle, J. Neubauer, and J. Suttle. 2011. Coordinate expression of AOS genes and JA accumulation: JA is not required for initiation of closing layer in wound healing tubers. Journal of Plant Physiology. doi:10.1016/jplph.2010.12.001.

    PubMed  Google Scholar 

  • Martin, M., J. León, C. Dammann, J.-P. Albar, G. Griffiths, and J.J. Sánchez-Serrano. 1999. Antisense-mediated depletion of potato leaf ω3 fatty acid desaturase lowers linolenic acid content and reduces gene activation in response to wounding. European Journal of Biochemistry 262: 283–290.

    Article  PubMed  CAS  Google Scholar 

  • Miersch, O., J. Neumerkel, M. Dippe, I. Stenzel, and C. Wasternack. 2008. Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. The New Phytologist 177: 114–127.

    PubMed  CAS  Google Scholar 

  • Mueller, M.J., L. Méne-Saffrané, C. Grun, K. Karg, and E.E. Farmer. 2006. Oxylipin analysis methods. The Plant Journal 45: 472–489.

    Article  PubMed  CAS  Google Scholar 

  • Pruski, K., T. Astatkie, P. Dupessis, T. Lewis, J. Nowak, and P.C. Struik. 2003. Use of jasmonates for conditioning of potato plantlets and microtubers in greenhouse production of minitubers. American Journal of Potato Research 80: 183–193.

    Article  CAS  Google Scholar 

  • Šmiko, I., E.A. Omer, E.E. Ewing, S. McMurry, J.L. Koch, and R.J. Davies. 1996. Tuberonic (12-OH-jasmonic) acid glucoside and its methyl ester in potato. Phytochemistry 43: 727–730.

    Article  Google Scholar 

  • Suttle, J.C. 2007. Dormancy and sprouting. In Potato biology and biotechnology: Advances and perspectives, ed. D. Vreugdenhil, J. Bradshaw, C. Gebhart, F. Govers, M.A. Taylor, D.K.L. MacKerron, and H.A. Ross, 237–256. Amsterdam: Elsevier.

    Google Scholar 

  • Suttle, J.C., and J.F. Hultstrand. 1994. Role of endogenous abscisic acid in potato microtuber dormancy. Plant Physiology 105: 891–896.

    PubMed  CAS  Google Scholar 

  • Świątek, A., M. Lenlou, D. Van Bockstaele, D. Inzé, and H. Van Onckelen. 2002. Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiology 128: 201–211.

    Article  PubMed  Google Scholar 

  • Wang, C.Y. 1998. Methyl jasmonate inhibits postharvest sprouting and improves storage quality of radishes. Postharvest Biology and Technology 14: 179–183.

    Article  Google Scholar 

  • Wasternack, C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100: 681–697.

    Article  PubMed  CAS  Google Scholar 

  • Weber, H., B.A. Vick, and E.E. Farmer. 1997. Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate family. Proceedings of the National Academy of Sciences U.S.A. 94: 10473–10478.

    Article  CAS  Google Scholar 

  • Yoshihara, T., E.A. Omer, H. Koshino, S. Sakamura, Y. Kikuta, and Y. Koda. 1989. Structure of a tuber-inducing stimulus from potato leaves (Solanum tuberosum L.). Agricultural and Biological Chemistry 53: 2835–2837.

    CAS  Google Scholar 

  • Zhang, Y., and J.G. Turner. 2008. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3: e3699.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey C. Suttle.

Additional information

Mention of company or trade name does not imply endorsement by the United States Department of Agriculture over others not named.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suttle, J.C., Huckle, L.L. & Lulai, E.C. The Effects of Dormancy Status on the Endogenous Contents and Biological Activities of Jasmonic Acid, N-(jasmonoyl)-Isoleucine, and Tuberonic Acid in Potato Tubers. Am. J. Pot Res 88, 283–293 (2011). https://doi.org/10.1007/s12230-011-9192-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12230-011-9192-5

Keywords

Navigation