The bicarbonate transporters in the solute carrier 4 (SLC4) family, found in all kingdoms of life, are important for the maintenance of acid-base homeostasis to regulate pH in the organelles, the cytosol, and the extracellular fluid. Their functions are tightly regulated in cells for their critical roles. Dysfunctions of SLC4 transporters lead to severe human diseases or disorders including blindness, short stature, abnormal cognitive function, cerebral calcification, metabolic acidosis, anemia, and hearing abnormalities. Although recent studies have revealed the structures of few SLC4 transporters, the mechanisms of transport and activity regulation of the SLC4 transporters are still obscure. We set out to answer these questions by investigating Arabidopsis thaliana Bor1 (AtBor1), a borate transporter in the SLC4 family. AtBor1 plays an important role in maintaining boron homeostasis in plants and is homologous to human SLC4 transporters. Using cryo-electron microscopy (cryoEM) single particle analysis, we determined the structure of the full-length AtBor1 dimer at 2.2 Å resolution. This structure not only shows the inward-facing conformation of the SLC4 transporters at an atomic resolution for the first time, but also reveals an unexpected inhibition domain at the C-terminus of AtBor1 that locks the conformation and blocks the substrate entrance and exit in a domain-swapped manner in the AtBor1 dimer. Mutagenesis and yeast complementation assays demonstrated that abolishing the binding of the C-terminal inhibition domain activated AtBor1, suggesting a novel autoinhibitory mechanism for the clade I type BOR-like transporters, which is further supported by our cryoEM structures of the active AtBor1. Both the inward-facing conformation and the long-sought-after occluded conformation are found in the structures of active AtBor1, providing unprecedented atomic details to explain the elevator transport mechanism of the SLC4 transporters.