Leaf miner (Cameraria ohridella) infestation drives progressive chloroplast degradation, thylakoid complex reorganization, and phenolic depletion in horse chestnut (Aesculus hippocastanum) leaves

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ABSTRACT Leaf-mining by Cameraria ohridella (Lepidoptera, Gracillariidae) impairs horse chestnut ( Aesculus hippocastanum ), yet the subcellular mechanisms underlying the progressive decline in photosynthesis remain insufficiently resolved. This study presents the first integrated multi-scale analysis of infestation effects across distinct leaf regions, healthy areas, intact areas surrounding mines, early- and late-stage mined areas, using light microscopy, transmission electron microscopy (TEM), photosynthetic pigment content determination, 77K fluorescence spectroscopy, blue-native polyacrylamide gel electrophoresis (BN-PAGE), Imaging PAM, gas exchange, and phenolic metabolite profiling. TEM revealed progressive chloroplast degradation, including thylakoid swelling, granum disorganization, increased plastoglobule size and number, culminating in vacuole-associated plastid remnants in late stages. Despite robust pigment losses, 77K fluorescence emission spectra and BN-PAGE showed roughly preserved thylakoid set-up with stable photosystem I/photosystem II (PSII) ratios but declines in PSII core to antenna ratio up to advanced infestation indicating structural persistence amid functional decay. F v /F m and electron transport rate declined progressively, while gas exchange indicated early non-stomatal limitations and late transpiration surges linked to necrosis. Non-photochemical quenching remained unchanged for a long time despite the declining PSII function. Phenolic profiles showed compound-specific accumulation in early stages but depletion in necrotic tissues, signaling metabolic exhaustion. Infestation triggers staged thylakoid remodeling linked to functional and metabolic shifts. Greater vulnerability of PSII relative to PSI establishes fluorescence imaging parameters as early diagnostic tools for urban tree management. These findings reveal a staged progression of subcellular and tissue-level responses, extending the mechanistic understanding of herbivory-induced chloroplast decline beyond the metabolite- or photosynthesis-focused scope of prior studies.

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