Stress-Induced Flowering in Pharbitis—A Review

DOI: 10.4236/ajps.2013.412A3009   PDF   HTML   XML   3,942 Downloads   5,441 Views   Citations


Many plant species are induced to flower by stress. Stress-induced flowering has been studied mostly in the short-day plant pharbitis (also called Japanese morning glory; Ipomoea nil, formerly Pharbitis nil). In this article, physiological characteristics, the regulation by salicylic acid (SA) and the expression of flowering-related genes in stress-induced flowering in pharbitis are reviewed. Pharbitis flowered under long-days in response to poor nutrition or low temperature. The pharbitis plants induced to flower by stress reached anthesis, fruited and produced fertile seeds. The progeny of the stressed plants developed normally. Grafting experiments indicated that a transmissible flowering stimulus is involved in poor nutrition stress-induced flowering. Aminooxyacetic acid (AOA), a phenylalanine ammonia-lyase (PAL) inhibitor, inhibited the stress-induced flowering, and this inhibition was overcome by SA. Stress induced PAL activity and SA biosynthesis. PnFT2, a pharbitis ortholog of the flowering gene FLOWERING LOCUS T of Arabidopsis thaliana, was expressed when the plants were induced to flower by stress. The overexpression of PnFT2 induced flowering, and PnFT2RNAi inhibited it. AOA inhibited PnFT2 expression induced by stress, and SA eliminated this inhibitory effect. SA enhanced PnFT2 expression under poor nutrition but not under non-stressful conditions. Therefore, stress may induce the production of SA and other unknown factor(s) that may work in combination to induce PnFT2 expression and flowering.

Share and Cite:

K. Wada, M. Yamada and K. Takeno, "Stress-Induced Flowering in Pharbitis—A Review," American Journal of Plant Sciences, Vol. 4 No. 12C, 2013, pp. 74-79. doi: 10.4236/ajps.2013.412A3009.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] B. Thomas and D. Vince-Prue, “Photoperiodism in Plants,” Academic Press, San Diego, 1997.
[2] K. C. Wada and K. Takeno, “Stress-Induced Flowering,” Plant Signaling and Behavior, Vol. 5, No. 8, 2010, pp. 1-4.
[3] K. C. Wada and K. Takeno, “Salicylic Acid-Mediated Stress-Induced Flowering,” In: S. Hayat, A. Ahmad and M. N. Alyemini, Eds., Salicylic Acid: Plant Growth and Development, Springer, New York, 2013, pp. 163-182.
[4] K. Takeno, “Stress-Induced Flowering,” In: P. Ahmad and M. N. V. Prasad, Eds., Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability, Springer, New York, 2012, pp. 331-345.
[5] M. Shinozaki and A. Takimoto, “Effects of Some Growth Regulators and Benzoic Acid Derivatives on Flower Initiation and Root Elongation of Pharbitis nil, Strain Kidachi,” Plant and Cell Physiology, Vol. 24, No. 3, 1983, pp. 433-439.
[6] M. Shinozaki, K. Asada and A. Takimoto, “Correlation between Chlorogenic Acid Content in Cotyledons and Flowering in Pharbitis Seedlings under Poor Nutrition,” Plant and Cell Physiology, Vol. 29, No. 4, 1988, pp. 605-609.
[7] M. Shinozaki, N. Hirai, Y. Kojima, K. Koshimizu and A.Takimoto, “Correlation between Level of Phenylpropanoids in Cotyledons and Flowering in Pharbitis Seedlings under High-fluence Illumination,” Plant and Cell Physiology, Vol. 35, No. 5, 1994, pp. 807-810.
[8] A. Ishimaru, K. Takeno and M. Shinozaki, “Correlation of Flowering Induced by Low Temperature and Endogenous Levels of Phenylpropanoids in Pharbitis nil: A Study with a Secondary-Metabolism Mutant,” Journal of Plant Physiology, Vol. 148, No. 6, 1996, pp. 672-676.
[9] T. Hatayama and K. Takeno, “The Metabolic Pathway of Salicylic Acid Rather than of Chlorogenic Acid Is Involved in the Stress-Induced Flowering of Pharbitis nil,” Journal of Plant Physiology, Vol. 160, No. 5, 2003, pp. 461-467.
[10] K. C. Wada, H. Kondo and K. Takeno, “Obligatory Short-Day Plant, Perilla frutescens var. crispa Can Flower in Response to Low-intensity Light Stress under Long-Day Conditions,” Physiologia Plantarum, Vol. 138, No. 3, 2010, pp. 339-345.
[11] A. Shimakawa, T. Shiraya, Y. Ishizuka, K. C. Wada, T. Mitsui and K. Takeno, “Salicylic Acid Is Involved in the Regulation of Starvation Stress-Induced Flowering in Lemna paucicostata,” Journal of Plant Physiology, Vol. 169, No. 10, 2012, pp. 987-991.
[12] C. Martínez, E. Pons, G. Prats and J. León, “Salicylic Acid Regulates Flowering Time and Links Defense Responses and Reproductive Development,” Plant Journal, Vol. 37, No. 2, 2004, pp. 209-217.
[13] J. Kolár and J. Seňková, “Reduction of Mineral Nutrient Availability Accelerates Flowering of Arabidopsis thaliana,” Journal of Plant Physiology, Vol. 165, No. 15, 2008, pp. 1601-1609.
[14] K. C. Wada, M. Yamada, T. Shiraya and K. Takeno, “Salicylic Acid and the Flowering Gene FLOWERING LOCUS T Homolog Are Involved in Poor-Nutrition Stress-Induced Flowering of Pharbitis nil,” Journal of Plant Physiology, Vol. 167, No. 6, 2010, pp. 447-452.
[15] M. Yamada and K. Takeno, “Stress and Salicylic Acid Induce the Expression of PnFT2 in the Regulation of the Stress-Induced Flowering of Pharbitis nil,” Journal of Plant Physiology, 2013.
[16] M. Shinozaki, “Organ Correlation in Long-Day Flowering of Pharbitis nil,” Biologia Plantarum, Vol. 27, No. 4-5, 1985, pp. 382-385.
[17] R. A. Dixon and L. Paiva, “Stress-Induced Phenylpropanoid Metabolism,” Plant Cell, Vol. 7, No. 7, 1995, pp. 1085-1097.
[18] I. M. Scott, S. M. Clarke, J. E. Wood and L. A. J. Mur, “Salicylate Accumulation Inhibits Growth at Chilling Temperature in Arabidopsis,” Plant Physiology, Vol. 135, No. 2, 2004, pp. 1040-1049.
[19] H. Kessmann, R. Edwards, P. W, Geno and R. A. Dixon, “Stress Responses in Alfalfa (Medicago sativa L.): V. Constitutive and Elicitor-induced Accumulation of Isoflavonoid Conjugates in Cell Suspension Cultures,” Plant Physiology, Vol. 94, No. 1, 1990, pp. 227-232.
[20] C. Appert, J. Zoń and N. Amrhein, “Kinetic Analysis of the Inhibition of Phenylalanine Ammonia-Lyase by 2-Aminoindan-2-phosphonic Acid and Other Phenylalanine Analogues,” Phytochemistry, Vol. 62, No. 3, 2003, pp. 415-422.
[21] K. C. Wada, “Regulatory Mechanism of Stress-Induced Flowering,” Ph.D. Dissertation, Niigata University, Niigata, 2012.
[22] C. F. Cleland and A. Ajami, “Identification of the Flower-Inducing Factor Isolated from Aphid Honeydew as Being Salicylic Acid,” Plant Physiology, Vol. 54, No. 6, 1974, pp. 904-906.
[23] C. F. Cleland, O. Tanaka and L. J. Feldman, “Influence of Plant Growth Substances and Salicylic Acid on Flowering and Growth in the Lemnaceae (duckweeds),” Aquatic Botany, Vol. 13, 1982, pp. 3-20.
[24] R. Kandeler, “Lemnaceae,” In: A. H. Halevy, Ed., CRC Handbook of Flowering, Vol. 3, CRC Press, Boca Raton, 1985, pp. 251-279.
[25] L. Corbesier and G. Coupland, “Photoperiodic Flowering of Arabidopsis: Integrating Genetic and Physiological Approaches to Characterization of the Floral Stimulus,” Plant and Cell Environment, Vol. 28, No. 1, 2005, pp. 54-66.
[26] P. K. Boss, R. M. Bastow, J. S. Mylne and C. Dean, “Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting,” Plant Cell, Vol. 16, No. S1, 2004, pp. S18-S31.
[27] R. Hayama, B. Agashea, E. Luleya, R. King and G. Coupland, “A Circadian Rhythm Set by Dusk Determines the Expression of FT Homologs and the Short-Day Photoperiodic Flowering Response in Pharbitis,” Plant Cell, Vol. 19, No. 10, 2007, pp. 2988-3000.
[28] J. Lee and I. Lee, “Regulation and Function of SOC1, a Flowering Pathway Integrator,” Journal of Experimental Botany, Vol. 61, No. 9, 2010, pp. 2247-2254.
[29] R. Amasino, “Seasonal and Developmental Timing of Flowering,” Plant Journal, Vol. 61, No. 6, 2010, pp. 1001-1013.
[30] F. Valverde, “CONSTANS and the Evolutionary Origin of Photoperiodic Timing of Flowering,” Journal of Experimental Botany, Vol. 62, No. 8, 2011, pp. 2453-2463.
[31] P. Suárez-López, K. Wheatley, F. Robson, H. Onouchi, F. Valverde and G. Coupland, “CONSTANS Mediates the Circadian Clock and the Control of Flowering in Arabidopsis,” Nature, Vol. 410, No. 6832, 2001, pp. 1116-1120.
[32] T. Izawa, T. Oikawa, N. Sugiyama, T. Tanisaka, M. Yano and K. Shimamoto, “Phytochrome Mediates the External Light Signal to Repress FT Orthologs in Photoperiodic Flowering of Rice,” Genes and Development, Vol. 16, No. 15, 2002, pp. 2006-2020.
[33] F. Valverde, A. Mouradov, W. Soppe, D. Ravenscroft, A. Samach and G. Coupland, “Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering,” Science, Vol. 303, No. 5660, 2004, pp. 1003-1006.
[34] I. G. Matsoukas, A. J. Massiah and B. Thomas, “Florigenic and Antiflorigenic Signaling in Plants,” Plant and Cell Physiology, Vol. 53, No. 11, 2012, pp. 1827-1842.
[35] J. Liu, J. Yu, L. McIntosh, H. Kende and J. A. D. Zeevaart, “Isolation of a CONSTANS Ortholog from Pharbitis nil and its Role in Flowering,” Plant Physiology, Vol. 125, No. 4, 2001, pp. 1821-1830.
[36] Y. Higuchi, K. Sage-Ono, R. Sasaki, N. Ohtsuki, A. Hoshino, S. Iida, H. Kamada and M. Ono, “Constitutive Expression of the GIGANTEA Ortholog Affects Circadian Rhythms and Suppresses One-Shot Induction of Flowering in Pharbitis nil, a Typical Short-Day Plant,” Plant and Cell Physiology, Vol. 52, No. 4, 2011, pp. 638-650.
[37] C. A. Dezar, J. I. Giacomelli, P. A. Manavella, D. A. Ré, M. Alves-Ferreira, I. T. Baldwin, G. Bonaventure and R. L. Chan, “HAHB10, a Sunflower HD-Zip II Transcription Factor, Participates in the Induction of Flowering and in the Control of Phytohormone-mediated Responses to Biotic Stress,” Journal of Experimental Botany, Vol. 62, No. 3, 2011, pp. 1061-1076.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.