Energy status-promoted growth and development of Arabidopsis require copper deficiency response transcriptional regulator SPL7

Abstract

Copper (Cu) is a cofactor of around 300 Arabidopsis proteins, including photosynthetic and mitochondrial electron transfer chain enzymes critical for adenosine triphosphate (ATP) production and carbon fixation. Plant acclimation to Cu deficiency requires the transcription factor SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE7 (SPL7). We report that in the wild type (WT) and in the spl7-1 mutant, respiratory electron flux via Cu-dependent cytochrome c oxidase is unaffected under both normal and low-Cu cultivation conditions. Supplementing Cu-deficient medium with exogenous sugar stimulated growth of the WT, but not of spl7 mutants. Instead, these mutants accumulated carbohydrates, including the signaling sugar trehalose 6-phosphate, as well as ATP and NADH, even under normal Cu supply and without sugar supplementation. Delayed spl7-1 development was in agreement with its attenuated sugar responsiveness. Functional TARGET OF RAPAMYCIN and SNF1-RELATED KINASE1 signaling in spl7-1 argued against fundamental defects in these energy-signaling hubs. Sequencing of chromatin immunoprecipitates combined with transcriptome profiling identified direct targets of SPL7-mediated positive regulation, including Fe SUPEROXIDE DISMUTASE1 (FSD1), COPPER-DEFICIENCY-INDUCED TRANSCRIPTION FACTOR1 (CITF1), and the uncharacterized bHLH23 (CITF2), as well as an enriched upstream GTACTRC motif. In summary, transducing energy availability into growth and reproductive development requires the function of SPL7. Our results could help increase crop yields, especially on Cu-deficient soils.