Abstract
d-Limonene induces expression of PDF1.2 gene and resistance against Colletotrichum higginsianum in Arabidopsis ecotype Col-0. The limonene-induced expression of PDF1.2 was diminished in jar1-1 (jasmonate resistant 1-1) plants, indicating that the response of Arabidopsis depends on jasmonic acid (JA)-regulated defense signaling pathway. In fact, systemic induction of PDF1.2 was confirmed when the Arabidopsis plants harboring the PDF1.2 promotor::GUS were exposed to limonene. A similar protective effect was also observed on Japanese mustard spinach (Brassica rapa var. perviridis) challenged with C. higginsianum, suggesting that plants are capable of recognizing gaseous limonene and activate disease resistance.
References
Blom D, Fabbri C, Connor EC, Schiest FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058
Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032
Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102
Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2006) ETR-, JAR- and PAD2-dependent signaling pathways are involved in C6-aldehyde-induced defense responses of Arabidopsis. Plant Sci 171:415–423
Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37
Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry 69:2127–2132
Marques JPR, Amorim L, Silva-Junior GJ, Spósito MB, Appezzato-da Gloria B (2015) Structural and biochemical characteristics of citrus flowers associated with defence against a fungal pathogen. AoB Plants 7:plu090. doi:10.1093/aobpla/plu090
Narusaka Y, Narusaka M, Abe H, Hosaka N, Kobayashi M, Shiraishi T, Iwabuchi M (2009) High-throughput screening for plant defense activators using a β-glucuronidase-reporter gene assay in Arabidopsis thaliana. Plant Biotech 26:345–349
Narusaka M, Minami T, Iwabuchi C, Hamasaki T, Takasaki S, Kawamura K, Narusaka Y (2015) Yeast cell wall extract induces disease resistance against bacterial and fungal pathogens in Arabidopsis thaliana and Brassica crop. PLoS One 10:e0115864. doi:10.1371/journal.pone.0115864
Naznin HA, Kiyohara D, Kimura M, Miyazawa M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by growth-promoting fungi in Arabidopsis thaliana. PLoS One 9:e86882. doi:10.1371/journal.pone.0086882
Singh G, Singh OP (2002) Chemistry of essential oils of Citrus species. Nat Prod Rad 1:8–21
Sun J (2007) d-Limonene: safety and clinical applications. Altern Med Rev 12:259–264
Toyoda K, Ikeda S, Morikawa J, Hirose M, Maeda A, Suzuki T, Inagaki Y, Ichinose Y, Shiraishi T (2013) The Medicago truncatula–Mycosphaerella pinodes interaction: a new pathosystem for dissecting fungal-suppressor-mediated disease susceptibility in plants. J Gen Plant Pathol 79:1–11
Yamagiwa Y, Inagaki Y, Ichinose Y, Toyoda K, Hyakumachi M, Shiraishi T (2011) Talaromyces wortmannii FS2 emits β-caryophyllene, which promotes plant growth and induces resistance. J Gen Plant Pathol 77:336–341
Yamasaki Y, Kunoh H, Yamamoto H, Akimitsu K (2007) Biological roles of monoterpene volatiles derived from rough lemon (Citrus jambhiri Lush) in citrus defense. J Gen Plant Pathol 73:168–179
Acknowledgments
We gratefully acknowledge Drs. Yoshihiro Narusaka and Mari Narusaka (Research Institute of Biological Sciences Okayama, Okayama, Japan) for their gift of Arabidopsis transgenic seeds harboring the PDF1.2 promotor-GUS (β-glucuronidase) fusion gene as the reporter gene. This research was in part supported by the Research Grant for Encouragement of Students to KF from the Graduate School of Natural Science and Technology, Okayama University, Japan.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10327_2015_621_MOESM1_ESM.docx
Supplementary Fig. 1 Direct effect of gaseous limonene on fungal development on ethanol-killed onion epidermal cells. A conidial suspension of Colletotrichum higginsianum (5 µL of 105 spores/mL) was dropped onto the surface of ethanol-killed onion epidermal cells in a glass vessel continuously filled with or without limonene. At 2 days after inoculation (2 dpi), germination (purple), appressorial formation (blue) and successful penetrations (yellow) were counted using a light microscope (see Fig. 1 in the text). Typical fungal development on the ethanol-killed epidermal cells in the absence or presence of limonene is shown on the right. s conidial spore, ap appressorium, ih infection hyphae. Bar indicates 50 μm. (DOCX 58 kb)
10327_2015_621_MOESM2_ESM.docx
Supplementary Fig. 2 Limonene-induced protective effect against Colletotrichum higginsianum in Arabidopsis thaliana at 6 days after inoculation (dpi). Five-week-old seedlings were treated for 24 h with or without limonene (100 µmol/L). At 1, 3 and 7 days after treatment, six 5-µL drops of a conidial suspension (106 spores/mL) were placed on each leaf (DOCX 91 kb)
Rights and permissions
About this article
Cite this article
Fujioka, K., Gotoh, H., Noumi, T. et al. Protection induced by volatile limonene against anthracnose disease in Arabidopsis thaliana . J Gen Plant Pathol 81, 415–419 (2015). https://doi.org/10.1007/s10327-015-0621-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-015-0621-z