Abstract
Alkaline/neutral invertases (NINVs), which irreversibly catalyze the hydrolysis of sucrose into fructose and glucose, play crucial roles in carbohydrate metabolism and plant development. Comprehensive insights into NINV genes are lacking in Salvia miltiorrhiza, a well-known traditional Chinese medicinal (TCM) plant with significant medicinal and economic value. Through genome-wide prediction, nine putative SmNINV genes, termed SmNINV1-SmNINV9, were identified. Integrated analysis of gene structures, sequence features, conserved domains, conserved motifs and phylogenetic trees revealed the conservation and divergence of SmNINVs. The identified SmNINVs were differentially expressed in roots, stems, leaves, flowers, and different root tissues. They also responded to drought, salicylic acid, yeast extract, and methyl jasmonate treatments. More importantly, computational prediction and experimental validation showed that SmNINV3 and SmNINV4 were targets of Smi-miR399, a conserved miRNA previously shown to affect Pi uptake and translocation through the cleavage of PHOSPHATE2 (PHO2). Consistently, analysis of 43 NINV genes and 26 miR399 sequences from Arabidopsis thaliana, Populus trichocarpa, Manihot esculenta, and Solanum lycopersicum showed that various AtNINV, PtNINV, MeNINV, and SlNINV genes were regulated by miR399. It indicates that the miR399-NINV module exists widely in plants. Furthermore, Smi-miR399 also cleaved SmPHO2 transcripts in S. miltiorrhiza, suggesting the complexity of NINVs, PHO2, and miR399 networks.
Highlights
In plants, invertases are pivotal enzymes involved in sucrose metabolism
The results showed that SmNINV5, SmNINV6, SmNINV7, and SmNINV8 were drought-responsive
The results showed that SmNINV3 and SmNINV4 were cleaved by
Summary
Invertases are pivotal enzymes involved in sucrose metabolism. They catalyze irreversible hydrolysis of sucrose into glucose and fructose [1,2]. AINVs are β-fructofuranosidases and N-glycosylated proteins with an optimal pH of 4.5–5.5, whereas NINVs consist of a novel family of glucosidases with optimal pH of 6.5–8.0. They are substantially distinct in evolutionary origins, and biochemical and molecular characteristics [3,4]. In contrast to AINVs, NINVs originated from cyanobacteria and are unique to plants and photosynthetic bacteria [13]. They locate in the cytosol and in multiple subcellular compartments, including the mitochondria, the chloroplasts, Plants 2019, 8, 490; doi:10.3390/plants8110490 www.mdpi.com/journal/plants
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