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

ABSTRACT: Miscanthus × giganteus is 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 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 C4 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.

SUBMITTER: Spence AK

PROVIDER: S-EPMC4085969 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsA clone of the hybrid perennial C4 grass Miscanthus × giganteus (Mxg) is known for achieving exceptionally high rates of leaf CO2 uptake during chilling. This is a requisite of success in the early spring, as is the ability of the leaves to survive occasional frosts. The aim of this study was to search for genotypes with greater potential than Mxg for photosynthesis and frost survival under these conditions.MethodsA total of 864 accessions representing 164 local populations of M. sacchariflorus (Msa), M. sinensis (Msi) and M. tinctorius (Mti) collected across Japan were studied. Accessions whose leaves survived a natural late frost in the field were screened for high maximum photosystem II efficiency (Fv/Fm) following chilling weather, as an indicator of their capacity for light-limited photosynthesis. Those showing the highest Fv/Fm were transferred to a high-light-controlled environment and maintained at chilling temperatures, where they were further screened for their capacities for high-light-limited and light-saturated leaf uptake of CO2 (ΦCO2,max and Asat, respectively).Key resultsFor the first time, relatives of Mxg with significantly superior capacities for photosynthesis at chilling temperatures were identified. Msa accession '73/2' developed leaves in the spring that survived night-time frost, and during growth under chilling maintained a statistically significant 79 % higher ΦCO2,max, as a measure of light-limited photosynthesis, and a 70 % higher Asat, as a measure of light-saturated photosynthesis. A second Msa accession, '73/3' also showed significantly higher rates of leaf uptake of CO2.ConclusionsAs remarkable as Mxg has proved in its chilling tolerance of C4 photosynthesis, this study shows that there is still value and potential in searching for yet more superior tolerance. Msa accession '73/2' shows rates of light-limited and light-saturated photosynthesis at chilling temperatures that are comparable with those of the most cold-tolerant C3 species. This adds further proof to the thesis that C4 photosynthesis is not inherently limited to warm climates.

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

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