Arabidopsis CURLY LEAF functions in leaf immunity against fungal pathogens by concomitantly repressing SEPALLATA3 and activating ORA59

• Published in: The Plant journal : for cell and molecular biology Vol. 108; no. 4; pp. 1005 - 1019
• Main Authors: Singkaravanit‐Ogawa, Suthitar, Kosaka, Ayumi, Kitakura, Saeko, Uchida, Kotaro, Nishiuchi, Takumi, Ono, Erika, Fukunaga, Satoshi, Takano, Yoshitaka
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.11.2021
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - immunology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Colletotrichum; Colletotrichum - physiology; Colletotrichum fungi; CURLY LEAF; Defensins; Flowering; Fungi; Gene Expression; Gene Expression Regulation, Plant; Homeodomain Proteins - genetics; Homeodomain Proteins - metabolism; Host plants; Immune response; Immunity; Leaves; Loss of Function Mutation; Microscopic analysis; Mutants; non‐host resistance; ORA59; Pathogens; plant defensins; Plant Diseases - immunology; Plant Diseases - microbiology; Plant Immunity; Plant Leaves - genetics; Plant Leaves - growth & development; Plant Leaves - immunology; plant morphogenesis; Plants; SEPALLATA3; Transcription Factors - genetics; Transcription Factors - metabolism; CURLY LEAF; plant defensins; plant morphogenesis; SEPALLATA3; Colletotrichum fungi; ORA59; non-host resistance
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15488

SUMMARY Arabidopsis non‐host resistance against non‐adapted fungal pathogens including Colletotrichum fungi consists of pre‐invasive and post‐invasive immune responses. Here we report that non‐host resistance against non‐adapted Colletotrichum spp. in Arabidopsis leaves requires CURLY LEAF (CLF), which is critical for leaf development, flowering and growth. Microscopic analysis of pathogen behavior revealed a requirement for CLF in both pre‐ and post‐invasive non‐host resistance. The loss of a functional SEPALLATA3 (SEP3) gene, ectopically expressed in clf mutant leaves, suppressed not only the defect of the clf plants in growth and leaf development but also a defect in non‐host resistance against the non‐adapted Colletotrichum tropicale. However, the ectopic overexpression of SEP3 in Arabidopsis wild‐type leaves did not disrupt the non‐host resistance. The expression of multiple plant defensin (PDF) genes that are involved in non‐host resistance against C. tropicale was repressed in clf leaves. Moreover, the Octadecanoid‐responsive Arabidopsis 59 (ORA59) gene, which is required for PDF expression, was also repressed in clf leaves. Notably, when SEP3 was overexpressed in the ora59 mutant background, C. tropicale produced clear lesions in the inoculated leaves, indicating an impairment in non‐host resistance. Furthermore, ora59 plants overexpressing SEP3 exhibited a defect in leaf immunity to the adapted Colletotrichum higginsianum. Since the ora59 plants overexpressing SEP3 did not display obvious leaf curling or reduced growth, in contrast to the clf mutants, these results strongly suggest that concomitant SEP3 repression and ORA59 induction via CLF are required for Arabidopsis leaf immunity to Colletotrichum fungi, uncoupled from CLF’s function in growth and leaf development. Significance Statement Leaves of Arabidopsis thaliana exhibit robust non‐host resistance against multiple and diverse microbial pathogens. Here, we report that Arabidopsis non‐host resistance requires CURLY LEAF (CLF), known to be critical for leaf morphogenesis and plant growth, and we reveal that the function of CLF in plant immunity is uncoupled from that in plant morphogenesis and growth.