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

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          Abstract

          Background

          SWEET 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).

          Results

          We 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.

          Conclusions

          We 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 material

          The online version of this article (doi:10.1186/s13068-016-0546-6) contains supplementary material, which is available to authorized users.

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          Most cited references34

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          The Sorghum bicolor genome and the diversification of grasses.

          Sorghum, an African grass related to sugar cane and maize, is grown for food, feed, fibre and fuel. We present an initial analysis of the approximately 730-megabase Sorghum bicolor (L.) Moench genome, placing approximately 98% of genes in their chromosomal context using whole-genome shotgun sequence validated by genetic, physical and syntenic information. Genetic recombination is largely confined to about one-third of the sorghum genome with gene order and density similar to those of rice. Retrotransposon accumulation in recombinationally recalcitrant heterochromatin explains the approximately 75% larger genome size of sorghum compared with rice. Although gene and repetitive DNA distributions have been preserved since palaeopolyploidization approximately 70 million years ago, most duplicated gene sets lost one member before the sorghum-rice divergence. Concerted evolution makes one duplicated chromosomal segment appear to be only a few million years old. About 24% of genes are grass-specific and 7% are sorghum-specific. Recent gene and microRNA duplications may contribute to sorghum's drought tolerance.
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            Sugar transporters for intercellular exchange and nutrition of pathogens.

            Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.
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              PGDD: a database of gene and genome duplication in plants

              Genome duplication (GD) has permanently shaped the architecture and function of many higher eukaryotic genomes. The angiosperms (flowering plants) are outstanding models in which to elucidate consequences of GD for higher eukaryotes, owing to their propensity for chromosomal duplication or even triplication in a few cases. Duplicated genome structures often require both intra- and inter-genome alignments to unravel their evolutionary history, also providing the means to deduce both obvious and otherwise-cryptic orthology, paralogy and other relationships among genes. The burgeoning sets of angiosperm genome sequences provide the foundation for a host of investigations into the functional and evolutionary consequences of gene and GD. To provide genome alignments from a single resource based on uniform standards that have been validated by empirical studies, we built the Plant Genome Duplication Database (PGDD; freely available at http://chibba.agtec.uga.edu/duplication/), a web service providing synteny information in terms of colinearity between chromosomes. At present, PGDD contains data for 26 plants including bryophytes and chlorophyta, as well as angiosperms with draft genome sequences. In addition to the inclusion of new genomes as they become available, we are preparing new functions to enhance PGDD.
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                Author and article information

                Contributors
                +81-29-838-6002 , hmizuno@affrc.go.jp
                skasuga@shinshu-u.ac.jp
                shiwak@affrc.go.jp
                Journal
                Biotechnol Biofuels
                Biotechnol Biofuels
                Biotechnology for Biofuels
                BioMed Central (London )
                1754-6834
                17 June 2016
                17 June 2016
                2016
                : 9
                : 127
                Affiliations
                [ ]Agrogenomics Research Center, National Institute of Agrobiological Sciences (NIAS), 2-1-2, Kannondai, Tsukuba, Ibaraki 305-8602 Japan
                [ ]Institute of Crop Science (NICS), National Agriculture and Food Research Organization, 1-2, Owashi, Tsukuba, Ibaraki 305-8602 Japan
                [ ]Faculty of Agriculture, Shinshu University, 8304 Minami-minowa, Nagano, 399-4598 Japan
                Article
                546
                10.1186/s13068-016-0546-6
                4912755
                27330561
                ee5a4d50-4f7a-451c-a7d2-3532da7330df
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 23 March 2016
                : 3 June 2016
                Funding
                Funded by: Kieikai Research Foundation
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Biotechnology
                phloem loading,phloem unloading,sugar transporter,bioethanol,rna-seq,snp,photosynthesis
                Biotechnology
                phloem loading, phloem unloading, sugar transporter, bioethanol, rna-seq, snp, photosynthesis

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