Evolution of cytosolic and organellar invertases empowered the colonization and thriving of land plants

The molecular innovation underpinning efficient carbon and energy metabolism during evolution of land plants remains largely unknown. Invertase-mediated sucrose cleavage into hexoses is central to fuel growth. Why some cytoplasmic invertases (CINs) function in the cytosol, whereas others operate in chloroplasts and mitochondria, is puzzling. We attempted to shed light on this question from an evolutionary perspective. Our analyses indicated that plant CINs originated from a putatively orthologous ancestral gene in cyanobacteria and formed the plastidic CIN (& alpha;1 clade) through endosymbiotic gene transfer, while its duplication in algae with a loss of its signal peptide produced the & beta; clade CINs in the cytosol. The mitochondrial CINs (& alpha;2) were derived from duplication of the plastidic CINs and coevolved with vascular plants. Importantly, the copy number of mitochondrial and plastidic CINs increased upon the emergence of seed plants, corresponding with the rise of respiratory, photosynthetic, and growth rates. The cytosolic CIN (& beta; subfamily) kept expanding from algae to gymnosperm, indicating its role in supporting the increase in carbon use efficiency during evolution. Affinity purification mass spectrometry identified a cohort of proteins interacting with & alpha;1 and 2 CINs, which points to their roles in plastid and mitochondrial glycolysis, oxidative stress tolerance, and the maintenance of subcellular sugar homeostasis. Collectively, the findings indicate evolutionary roles of & alpha;1 and & alpha;2 CINs in chloroplasts and mitochondria for achieving high photosynthetic and respiratory rates, respectively, which, together with the expanding of cytosolic CINs, likely underpin the colonization of land plants through fueling rapid growth and biomass production. The diversification and expansion of cytosolic and organellar invertases represent a key molecular innovation underpinning efficient carbon and energy metabolism for the evolution of land plants.

Automated summary

The origin and function of different types of invertase enzymes in land plants were investigated. Plastidic and mitochondrial invertases play roles in achieving high photosynthetic and respiratory rates, while cytosolic invertases are important for increasing carbon utilization efficiency. These invertases originated from ancestral genes in cyanobacteria and evolved through gene duplication and transfer processes.