A novel Arabidopsis thaliana protein, ABAP1 INTERACTING PROTEIN 10, mediates crosstalk between the cell cycle and primary metabolism

Plants have developed a sophisticated regulatory network that coordinates gene expression in meristematic zones in response to environmental conditions. Here, we identified a protein in Arabidopsis (Arabidopsis thaliana) that interacts with Armadillo BTB Arabidopsis protein 1 (ABAP1), a negative regulator of the cell cycle in plants. We characterized ABAP1 Interacting Protein (named AIP10) investigating its role in modulating plant development. T-DNA insertion lines with silenced expression of AIP10 were evaluated phenotypically (morphology, fresh and dry weight), via transcriptomics analyses (RNA-seq and RT-qPCR), physiologically (biochemically, Fluorcam and Li- COR), and metabolically (ATR-FTIR). We showed that AIP10 integrates cell division rates with transcriptional and primary metabolism reprogramming, through its protein interactions with ABAP1 and KIN10, a subunit of SnRK1 (Sucrose non-fermenting-1- related protein kinase 1). ABAP1 levels and activity were reduced in the absence of AIP10, licensing cell cycle progression for longer periods, which culminated in increased rates of cell division that boosted vegetative and reproductive growth. AIP10 silencing triggered a major transcriptional reprogramming of plant primary metabolism, possibly through SnRK1 regulation. aip10 mutants showed increased photosynthetic efficiency, as well as boosted carbon fixation, leading to increased biomass, seed productivity, and higher contents of proteins, lipids (triglycerides), and carbohydrates. Finally, we propose that the modulation of AIP10 expression is part of a mechanism that coordinates higher rates of cell division with better photosynthetic performance and carbon fixation to metabolically meet the plant energy demand, allowing the generation of plants with increased biomass and productivity. One-sentence summaryABAP1 INTERACTING PROTEIN10 connects the cell cycle and plant metabolism, with its silencing leading to increased cell division, carbon fixation, and metabolite levels in Arabidopsis.