Transcriptional responses indicate maintenance of photosynthetic proteins as key to the exceptional chilling tolerance of C4 photosynthesis inMiscanthus×giganteus

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Abstract

Miscanthus×giganteusis exceptional among C4 plants in its ability to acclimate to chilling (≤14 °C) and maintain a high photosynthetic capacity, in sharp contrast to maize, leading to very high productivity even in cool temperate climates. To identify the mechanisms that underlie this acclimation, RNA was isolated fromM×giganteusleaves in chilling and nonchilling conditions and hybridized to microarrays developed for its close relativeZea mays. Among 21 000 array probes that yielded robust signals, 723 showed significant expression change under chilling. Approximately half of these were for annotated genes. Thirty genes associated with chloroplast membrane function were all upregulated. Increases in transcripts for thelhcb5(chlorophyll a/b-binding protein CP26),ndhF(NADH dehydrogenase F, chloroplast),atpA(ATP synthase alpha subunit),psbA(D1),petA(cytochrome f), andlhcb4(chlorophyll a/b-binding protein CP29), relative to housekeeping genes inM.×giganteus, were confirmed by quantitative reverse-transcription PCR. In contrast,psbo1,lhcb5,psbA, andlhcb4were all significantly decreased inZ. maysafter 14 days of chilling. Western blot analysis of the D1 protein and LHCII type II chlorophyll a/b-binding protein also showed significant increases inM.×giganteusduring chilling and significant decreases inZ. mays. Compared to other C4 species,M.×giganteusgrown in chilling conditions appears to counteract the loss of photosynthetic proteins and proteins protecting photosystem II typically observed in other species by increasing mRNA levels for their synthesis.

C4 photosynthesis is impaired typically by chilling, but not in Miscanthus × giganteus. Global transcript profiling reveals that expression of many key photosynthetic genes is maintained or upregulated during chilling in M. × giganteus, in contrast to maize, suggesting a basis for chilling-tolerant C4 photosynthesis.

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