A linker histone acts as a transcription factor to orchestrate malic acid accumulation in apple in response to sorbitol

High carbohydrate availability promotes malic acid accumulation in fleshy fruits, but the underlying mechanism is not known. Here, we show that antisense repression of ALDOSE-6-PHOSPHATE REDUCTASE in apple (Malus domestica) decreases the concentrations of sorbitol and malate and the transcript levels of several genes involved in vacuolar malate transport, including the aluminum-activated malate transporter (ALMT) gene MdALMT9 (Ma1), the P-ATPase gene MdPH5, the MYB transcription factor gene MdMYB73, and the cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1, in fruit and leaves. We identified a linker histone H1 variant, MdH1.1, which complements the Arabidopsis (Arabidopsis thaliana) H1 deficient mutant and functions as a transcription factor. MdH1.1 activates MdMYB73, MdCIbHLH1, and MdPH5 expression by directly binding to their promoters. MdMYB73, in return, binds to the promoter of MdH1.1 to enhance its transcription. This MdH1.1-MdMYB73 feedback loop responds to sorbitol, regulating Ma1 expression. Antisense suppression of either MdH1.1 or MdMYB73 expression significantly decreases whereas overexpression increases Ma1 expression and malate accumulation. These findings demonstrate that MdH1.1, in addition to being an architectural protein for chromatin structure, operates as a transcription factor orchestrating malic acid accumulation in response to sorbitol, revealing how sugar signaling modulates vacuolar malate transport via a linker histone in plants.