Cracking vacuolar fumarate and malate transport shows its function in Arabidopsis metabolism and growth

ABSTRACT Malate and fumarate constitute a significant transient carbon stock that is dynamically synthesized during the photoperiod. These organic acids are diurnally stored and remobilised from the vacuole, and they have a key role in the cellular metabolic regulation. This function is well known in C4 and CAM plants. However, in C3 species that are the majority of terrestrial plants, the importance of the vacuolar accumulation/release and its influence on plant growth is still an open question. In Here we addressed this issue generating multiple knockout mutants in Arabidopsis thaliana lacking vacuolar anion channels of the Aluminium-Activated Malate Transporter (ALMT) family, to impair malate and fumarate transport to the vacuole. We show that in these mutants reducing vacuolar transport of malate and fumarate in mesophyll cells leads to a dramatic growth impairment. Metabolic and fluxomic analysis revealed that vacuolar malate and fumarate transport influences plant carbon and nitrogen metabolism as well as cellular pH and ionic homeostasis. In conclusion, our results show that the transport organic acids like malate and fumarate across the vacuolar membrane is essential for plant growth in a C3 plant too. These results establish the importance of the vacuolar pools of malate and fumarate in plant metabolism.