Comparative analysis of sucrose phosphate synthase (SPS) gene family between Saccharum officinarum and Saccharum spontaneum

Abstract

Background: Sucrose phosphate synthase (SPS) genes play vital roles in sucrose production across various plant species. Modern sugarcane cultivar is derived from the hybridization between the high sugar content species Saccharum officinarum and the high stress tolerance species Saccharum spontaneum, generating one of the most complex genomes among all crops. The genomics of sugarcane SPS remains under-studied despite its profound impact on sugar yield.

Results: In the present study, 8 and 6 gene sequences for SPS were identified from the BAC libraries of S. officinarum and S. spontaneum, respectively. Phylogenetic analysis showed that SPSD was newly evolved in the lineage of Poaceae species with recently duplicated genes emerging from the SPSA clade. Molecular evolution analysis based on Ka/Ks ratios suggested that polyploidy reduced the selection pressure of SPS genes in Saccharum species. To explore the potential gene functions, the SPS expression patterns were analyzed based on RNA-seq and proteome dataset, and the sugar content was detected using metabolomics analysis. All the SPS members presented the trend of increasing expression in the sink-source transition along the developmental gradient of leaves, suggesting that the SPSs are involved in the photosynthesis in both Saccharum species as their function in dicots. Moreover, SPSs showed the higher expression in S. spontaneum and presented expressional preference between stem (SPSA) and leaf (SPSB) tissue, speculating they might be involved in the differentia of carbohydrate metabolism in these two Saccharum species, which required further verification from experiments.

Conclusions: SPSA and SPSB genes presented relatively high expression and differential expression patterns between the two Saccharum species, indicating these two SPSs are important in the formation of regulatory networks and sucrose traits in the two Saccharum species. SPSB was suggested to be a major contributor to the sugar accumulation because it presented the highest expressional level and its expression positively correlated with sugar content. The recently duplicated SPSD2 presented divergent expression levels between the two Saccharum species and the relative protein content levels were highest in stem, supporting the neofunctionalization of the SPSD subfamily in Saccharum.

Keywords: BAC libraries; Metabolites; Polyploidy; S. officinarum; S. spontaneum; Sucrose phosphate synthase (SPS); Sugarcane; Transcriptome.

Fig. 1

Gene structure (a) and multiple alignment analysis (b) of SPS. Ss and So indicate two Saccharum species, including S. spontaneum and S. officinarum, respectively. For Fig. 2b, regions of interest were masked with red rectangles: light regulated phosphoserine (I), putative F-6-P binding site (II), 14–3-3 regulated phosphoserine and UDP-G binding domain (III), the osmotically regulated phosphoserine (IV) and various aspartate-proline pairs (DP motif, V, VI, VII)

Fig. 2

Evolutionary analysis of SPS family. a The distribution of SPS subfamilies in different plants. b Phylogenetic analysis of SPS gene family in different plants including S. bicolor, S. officinarum, S. spontaneum, Zea mays, Oryza sativa, Arabidopsis thaliana, Vitis vinifera, Brachypodium distachyon, Ananas comosus and Amborella trichopoda. c Ka/Ks values of the SPS subfamilies

Fig. 3

Expression profiles of SPS genes in various samples in two Saccharum species. Seedling, preM and M represent three developmental states: seedling, pre-mature and mature. In each stage, samples include leaves and internodes

Fig. 4

Expression profiles of SPS genes in gradient developmental leaves in two Saccharum species. Leaf samples in the seedling stage were divided into four gradient intervals (a basal zone, sink tissue; a transitional zone, going through the sink-source transition; a maturing zone and a mature zone, active C4 photosynthetic zones), including 15 segments (sec1 to sec15). a The heat map showing the expression levels of all SPS genes. s. b Comparative analysis of the trends in expression of the two species in gradient developmental leaves

Fig. 5

The relatively content of SPS protein in gradient developmental leaves (a) and stems (b) in two Saccharum species. The developmental leaves and stems were all divided into three developmental blocks: basal-zone (basal-z), maturing-zone (maturing-z), mature-zone (mature-zone)

Fig. 6

Metabolomics analysis in gradient developmental leaves (a) and stems (b) in two Saccharum species. The sampling methods are consistent with the proteomics analysis. The comparative analysis of the metabolites of sucrose and fructose-6-phosphatein in leaves and stem internodes of two species were performed, Fructose − 6-phosphate was not detected in the stems of either species