The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling

Abstract

BackgroundSWEET is a newly identified family of sugar transporters. Although SWEET transporters have been characterized by using Arabidopsis and rice, very little knowledge of sucrose accumulation in the stem region is available, as these model plants accumulate little sucrose in their stems. To elucidate the expression of key SWEET genes involved in sucrose accumulation of sorghum, we performed transcriptome profiling by RNA-seq, categorization using phylogenetic trees, analysis of chromosomal synteny, and comparison of amino acid sequences between SIL-05 (a sweet sorghum) and BTx623 (a grain sorghum).ResultsWe identified 23 SWEET genes in the sorghum genome. In the leaf, SbSWEET8-1 was highly expressed and was grouped in the same clade as AtSWEET11 and AtSWEET12 that play a role in the efflux of photosynthesized sucrose. The key genes in sucrose synthesis (SPS3) and that in another step of sugar transport (SbSUT1 and SbSUT2) were also highly expressed, suggesting that sucrose is newly synthesized and actively exported from the leaf. In the stem, SbSWEET4-3 was uniquely highly expressed. SbSWEET4-1, SbSWEET4-2, and SbSWEET4-3 were categorized into the same clade, but their tissue specificities were different, suggesting that SbSWEET4-3 is a sugar transporter with specific roles in the stem. We found a putative SWEET4-3 ortholog in the corresponding region of the maize chromosome, but not the rice chromosome, suggesting that SbSWEET4-3 was copied after the branching of sorghum and maize from rice. In the panicle from the heading through to 36 days afterward, SbSWEET2-1 and SbSWEET7-1 were expressed and grouped in the same clade as rice OsSWEET11/Xa13 that is essential for seed development. SbSWEET9-3 was highly expressed in the panicle only just after heading and was grouped into the same clade as AtSWEET8/RPG1 that is essential for pollen viability. Five of 23 SWEET genes had SNPs that caused nonsynonymous amino acid substitutions between SIL-05 and BTx623.ConclusionsWe determined the key SWEET genes for technological improvement of sorghum in the production of biofuels: SbSWEET8-1 for efflux of sucrose from the leaf; SbSWEET4-3 for unloading sucrose from the phloem in the stem; SbSWEET2-1 and SbSWEET7-1 for seed development; SbSWEET9-3 for pollen nutrition.Electronic supplementary materialThe online version of this article (doi:10.1186/s13068-016-0546-6) contains supplementary material, which is available to authorized users.

Roles of Aquaporins in Setaria viridis Stem Development and Sugar Storage

“…Of those 41 aquaporins the expression of 16, primarily NIPs and TIPs, was relatively low. However, PIP1;2, PIP2;1 , and NIP2;2 homologs were all highly expressed in pith and rind of sorghum plants after heading, which is consistent with our findings for the S. viridis homologs of these genes ( Figure 2 ; Mizuno et al, 2016). Comparisons with other gene expression studies for C 4 grass stem tissues were not possible as in most studies the internode tissue has not been separated into different developmental zones or the study has not reported aquaporin expression (Carson and Botha, 2000, 2002; Casu et al, 2007).…”

“…In mature S. viridis internode tissues, the transcript levels of TIPs and NIPs was generally low with the exception of SvNIP2;2, SvTIP4;2 , and SvTIP1;2. In a sorghum stem transcriptome report investigating SWEET gene involvement in sucrose accumulation, we note that transcripts for all 41 sorghum aquaporins were detected in pith and rind tissues in 60-day-old plants (Reddy et al, 2015; Mizuno et al, 2016). Of those 41 aquaporins the expression of 16, primarily NIPs and TIPs, was relatively low.…”

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

“…Particularly, SbTST4‐1 expression in RIO was dramatically higher than those in R9188/BTx406. Comparison of SbSUT2 and SbTST4‐1 expression patterns between the three genotypes, together with similar expression profiles in other sweet sorghum lines (Bihmidine et al ., ; Mizuno et al ., ), strongly indicated roles in sucrose import for stem storage sink (Figure S20). For SWEET s, 16 genes were expressed with Sb SWEET7‐1 (Sobic.007G191200) introgressed from BTx406 into R9188.…”

Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit

“…Concomitant with the genetic and biochemical characterization of transporters, there have been correlative studies hinting at the contribution of transporter gene expression to sugar content in sink tissue. For example, transcriptomic analyses of fruit development in apple (Wei et al ., ), grape (Afoufa‐Bastien et al ., ), pear (Li et al ., ), banana (Miao et al ., ) and tomato (Reuscher et al ., ; Feng et al ., ), as well as the development of sweet sorghum stems (Mizuno et al ., ) and sugar beet roots (Jung et al ., ), all point to members of sugar transporter families in which expression patterns coincide with sugar accumulation patterns. A combined proteomic and transcriptomic study of sugar beet tonoplast membranes led to the identification and characterization of BvTST (tonoplast sugar transporter), which is likely to be responsible for the high sucrose accumulation characteristic of sugar beet roots (Jung et al ., ), and which functions in consort with the leaf phloem‐localized sucrose loading transporter BvSUT in determining a source–sink interaction influenced by respective push and pull transporters (Nieberl et al ., ).…”