Abstract
In addition to conspicuous large mesophyll chloroplasts, where most photosynthesis occurs, small epidermal chloroplasts have also been observed in plant leaves. However, the functional significance of this small organelle remains unclear. Here, we present evidence that Arabidopsis epidermal chloroplasts control the entry of fungal pathogens. In entry trials, specialized fungal cells called appressoria triggered dynamic movement of epidermal chloroplasts. This movement is controlled by common regulators of mesophyll chloroplast photorelocation movement, designated as the epidermal chloroplast response (ECR). The ECR occurs when the PEN2 myrosinase-related higher-layer antifungal system becomes ineffective, and blockage of the distinct steps of the ECR commonly decreases preinvasive nonhost resistance against fungi. Furthermore, immune components were preferentially localized to epidermal chloroplasts, contributing to antifungal nonhost resistance in the pen2 background. Our findings reveal that atypical small chloroplasts act as defense-related motile organelles by specifically positioning immune components in the plant epidermis, which is the first site of contact between the plant and pathogens. Thus, this work deepens our understanding of the functions of epidermal chloroplasts.
Highlights
In addition to conspicuous large mesophyll chloroplasts, where most photosynthesis occurs, small epidermal chloroplasts have been observed in plant leaves
The effects of epidermal chloroplast response (ECR) impairment by CHUP1 overexpression and mutation on preinvasive nonhost resistance (NHR) were greater in edr[1] pen[2] double mutants than in pen[2] single mutants. These results demonstrate that the ECR contributes to preinvasive NHR against Colletotrichum fungi at the lower layer of PEN2-related immunity, while the breakdown of additional EDR1-related preinvasive defense has a greater impact on ECR-mediated immunity
Typical large mesophyll chloroplasts are important plant organelles that are responsible for photosynthesis
Summary
In addition to conspicuous large mesophyll chloroplasts, where most photosynthesis occurs, small epidermal chloroplasts have been observed in plant leaves. In entry trials, specialized fungal cells called appressoria triggered dynamic movement of epidermal chloroplasts. This movement is controlled by common regulators of mesophyll chloroplast photorelocation movement, designated as the epidermal chloroplast response (ECR). Our findings reveal that atypical small chloroplasts act as defense-related motile organelles by positioning immune components in the plant epidermis, which is the first site of contact between the plant and pathogens. Multiple immune components, including as-yet unknown factors, support the deployment of epidermal NHR against the entry of nonadapted fungal pathogens in Arabidopsis. The functional significance of small epidermal chloroplasts remains unclear
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