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The timing of flowering is tightly controlled by signals that integrate environmental and endogenous cues. Sugars produced by carbon fixation in the chloroplast are a crucial endogenous cue for floral initiation. Chloroplasts also convey information directly to the nucleus through retrograde signaling to control plant growth and development. Here, we show that mutants defective in chlorophyll biosynthesis and chloroplast development flowered early, especially under long-day conditions, although low sugar accumulation was seen in some mutants. Plants treated with the bleaching herbicide norflurazon also flowered early, suggesting that chloroplasts have a role in floral repression. Among retrograde signaling mutants, the golden2-like 1 (glk1) glk2 double mutants showed early flowering under long-day conditions. This early flowering was completely suppressed by constans (co) and flowering locus t (ft) mutations. Leaf vascular-specific knockdown of both GLK1 and GLK2 phenocopied the glk1 glk2 mutants. GLK1 and GLK2 repress flowering by directly activating the expression of B-BOX DOMAIN PROTEIN 14 (BBX14), BBX15, and BBX16 via CCAATC cis-elements in the BBX genes. BBX14/15/16 physically interact with CO in the nucleus, and expression of BBXs hampered CO-mediated FT transcription. Simultaneous knockdown of BBX14/15/16 by artificial miRNA (35S::amiR-BBX14/15/16) caused early flowering with increased FT transcript levels, whereas BBX overexpression caused late flowering. Flowering of glk1/2 and 35S::amiR-BBX14/15/16 plants was insensitive to norflurazon treatment. Taking these observations together, we propose that the GLK1/2-BBX14/15/16 module provides a novel mechanism explaining how the chloroplast represses flowering to balance plant growth and reproductive development.
Susila et al. (Mon,) studied this question.