The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production

• Published in: The Plant journal : for cell and molecular biology Vol. 54; no. 3; pp. 481 - 495
• Main Authors: Ishihara, Atsushi, Hashimoto, Yumi, Tanaka, Chihiro, Dubouzet, Joseph G., Nakao, Takahito, Matsuda, Fumio, Nishioka, Takaaki, Miyagawa, Hisashi, Wakasa, Kyo
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.05.2008; Blackwell Science
• Subjects: Anthranilate Synthase - genetics; Anthranilate Synthase - metabolism; Aromatic-L-Amino-Acid Decarboxylases - genetics; Aromatic-L-Amino-Acid Decarboxylases - metabolism; Ascomycota - growth & development; Biological and medical sciences; Botany; Cellular biology; Crop diseases; Fundamental and applied biological sciences. Psychology; Fungal plant pathogens; Gramineae; Metabolism; Molecular Structure; Mutation; Oryza - genetics; Oryza - metabolism; Oryza - microbiology; Oryza sativa; Pathology, epidemiology, host-fungus relationships. Damages, economic importance; physical defense; Phytopathology. Animal pests. Plant and forest protection; Plant Leaves - genetics; Plant Leaves - metabolism; Plant Leaves - microbiology; Plant Proteins - genetics; Plant Proteins - metabolism; Plants, Genetically Modified; Rice; secondary metabolism; serotonin; Serotonin - chemistry; Serotonin - metabolism; Signal Transduction - physiology; tryptophan; Tryptophan - chemistry; Tryptophan - metabolism; Monocotyledones; Decarboxylase; Anthranilate synthase; Growth; Enzyme; Lyases; Plant leaf; rice; Cell wall; Oxo-acid-lyases; Oryza sativa; Carbon-carbon lyases; serotonin; Gramineae; Carboxy-lyases; Angiospermae; physical defense; Spermatophyta; Mutation; Secondary metabolism; tryptophan
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/j.1365-313X.2008.03441.x

Summary The upregulation of the tryptophan (Trp) pathway in rice leaves infected by Bipolaris oryzae was indicated by: (i) enhanced enzyme activity of anthranilate synthase (AS), which regulates metabolic flux in the Trp pathway; (ii) elevated levels of the AS (OASA2, OASB1, and OASB2) transcripts; and (iii) increases in the contents of anthranilate, indole, and Trp. The measurement of the contents of Trp‐derived metabolites by high‐performance liquid chromatography coupled with tandem mass spectrometry revealed that serotonin and its hydroxycinnamic acid amides were accumulated in infected leaves. Serotonin accumulation was preceded by a transient increase in the tryptamine content and by marked activation of Trp decarboxylase, indicating that enhanced Trp production is linked to the formation of serotonin from Trp via tryptamine. Feeding of radiolabeled serotonin to inoculated leaves demonstrated that serotonin is incorporated into the cell walls of lesion tissue. The leaves of a propagating‐type lesion mimic mutant (sl, Sekiguchi lesion) lacked both serotonin production and deposition of unextractable brown material at the infection sites, and showed increased susceptibility to B. oryzae infection. Treating the mutant with serotonin restored deposition of brown material at the lesion site. In addition, the serotonin treatment suppressed the growth of fungal hyphae in the leaf tissues of the sl mutant. These findings indicated that the activation of the Trp pathway is involved in the establishment of effective physical defenses by producing serotonin in rice leaves.