Transcriptional responses indicate maintenance of photosynthetic proteins as key to the exceptional chilling tolerance of C ₄ photosynthesis in Miscanthus × giganteus

Summary

C ₄ 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 C ₄ photosynthesis.

Abstract

Miscanthus × giganteus is exceptional among C ₄ 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 from M × giganteus leaves in chilling and nonchilling conditions and hybridized to microarrays developed for its close relative Zea 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 the lhcb5 (chlorophyll a/b-binding protein CP26), ndhF (NADH dehydrogenase F, chloroplast), atpA (ATP synthase alpha subunit), psbA (D1), petA (cytochrome f), and lhcb4 (chlorophyll a/b-binding protein CP29), relative to housekeeping genes in M. × giganteus, were confirmed by quantitative reverse-transcription PCR. In contrast, psbo1, lhcb5, psbA, and lhcb4 were all significantly decreased in Z. mays after 14 days of chilling. Western blot analysis of the D1 protein and LHCII type II chlorophyll a/b-binding protein also showed significant increases in M. × giganteus during chilling and significant decreases in Z. mays. Compared to other C ₄ species, M. × giganteus grown 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.