Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond

In higher plants, invertases hydrolyze sucrose (Suc), the major end product of photosynthesis, into glucose (Glc) and fructose (Fru), which are used as nutrients, energy sources, and signaling molecules for plant growth, yield formation, and stress responses. The invertase enzymes, named CWINs, VINs, and CINs, are located in the cell wall, vacuole, and cytosol, respectively. We hypothesize, based on their distinctive subcellular locations and physiological roles, that invertases may have undergone different modes during evolution with important functional implications. Here, we provide phylogenetic and functional genomic evidence that CINs are evolutionarily and functionally more stable compared with CWINs and VINs, possibly reflecting their roles in maintaining cytosolic sugar homeostasis for cellular function, and that CWINs have coevolved with the vasculature, likely as a functional component of phloem unloading. Invertase-mediated Suc metabolism and sugar signaling have major roles in plant development and yield formation. During evolution, two structurally unrelated invertases evolved: neutral/alkaline invertases, also called cytoplasmic invertases (CINs), and acid invertases, either a form tightly bound to the cell wall (CWIN) or a soluble form residing in the vacuole (VIN). In vascular plants, CWINs have an essential role in phloem unloading and the development of nonphotosynthetic organs (sinks), while VINs generally contribute to sugar accumulation and cell expansion. By comparison, less is known about CINs. Recent studies have provided new insights into the control of plant fertility and fitness by VINs and CWINs and the structure of CINs and their post-translational regulation.