Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond

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. 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. 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. an acid invertase that has lost its ‘normal’ function to hydrolyze Suc owing to mutation of Asp 239. The mutation may result in the protein acting as a fructan exohydrolases, based on in vitro analyses of the recombinant protein. an acid invertase that lacks the complete residues of either of the two domains (NDPN and WECP/VDF), which are essential for the catalytic activity of acid invertase. a nonsynonymous substitution is a nucleotide mutation that alters the amino acid sequence of a protein. A synonymous substitution is nucleotide mutation that does not result in a change in amino acid sequence, hence generally does not affect the function of the encoded protein. DNA sequences that share a certain level of identity or similarity with that of normal invertases but with their open reading frames interrupted by stop codons, frameshifts, or truncations or even lacking a start codon. Pseudogenes may have some biological roles and evolutionary history, because they often share ancestry with their functional counterparts. (also called negative selection) refers to selection against nonsynonymous substitutions at the DNA level. In this case, the evolutionary distance based on synonymous substitutions is expected to be greater than the distance based on nonsynonymous substitutions. Purifying selection conserves important functional genetic features over time by selective pressure against deleterious variants to ensure the normal function of an organism or its population.