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Leaf growth is sustained by successive phases of cell proliferation and expansion that determine the final organ size. The rate and extension of these phases are modulated by several developmental and environmental cues. We show herein that changes in the redox status of tobacco chloroplasts caused by introduction of the alternative electron shuttle flavodoxin led to decreased leaf size. Flavodoxin activity as electron sink prevented over-reduction of the photosynthetic electron transport chain and propagation of reactive oxygen species. These effects correlated with significantly lower rates of cell expansion in leaves of flavodoxin-expressing plants. Neither the duration of the expansion phase nor the rate and extension of the proliferative stage were affected by the presence of the alternative electron carrier, resulting in smaller leaf cells without significant differences in their numbers. Cells from transformed plants contained fewer chloroplasts of wild-type size, but their cellular coverage was increased due to cell size reduction. Chloroplast redox modulation of leaf development was associated to increased proteasomal activity and lower endoreduplication. The results identify a new player in the global regulation of plant organ growth, as represented by plastid-generated redox signals, and underscore the value of alternative electron shuttles to investigate the signaling role of chloroplast oxido-reductive biochemistry in plant developmental pathways. Competing Interest Statement The authors have declared no competing interest.

The ability of plants to maintain photosynthesis in a dynamically changing environment is of central importance for their growth. As their photosynthetic machinery typically cannot adapt rapidly to fluctuations in the intensity of radiation, the level of photosynthetic efficiency is not always optimal. Cyanobacteria, algae, non-vascular plants (mosses and liverworts) and gymnosperms all produce flavodiirons (Flvs), a class of proteins not represented in the angiosperms; these proteins act to mitigate the photoinhibition of photosystem I. Here, genes specifying two cyanobacterial Flvs have been expressed in the chloroplasts of Arabidopsis thaliana in an attempt to improve the robustness of Photosystem I (PSI). The expression of Flv1 and Flv3 together shown to enhance the efficiency of the utilization of light and to boost the plants capacity to accumulate biomass. Based on an assessment of the chlorophyll fluorescence in the transgenic plants, the implication was that photosynthetic activity (including electron transport flow and non-photochemical quenching during a dark-to-light transition) was initiated earlier in the transgenic than in wild type plants. The improved photosynthetic performance of the transgenics was accompanied by an increased production of ATP, an acceleration of carbohydrate metabolism and a more pronounced partitioning of sucrose into starch. The indications are that Flvs are able to establish an efficient electron sink downstream of PSI, thereby ensuring that the photosynthetic electron transport chain remains in a more oxidized state. The expression of Flvs in a plant acts to both protect photosynthesis and to control the ATP/NADPH ratio; together, their presence is beneficial for the plants growth potential.