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      Root lodging is a physical stress that changes gene expression from sucrose accumulation to degradation in sorghum

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          Abstract

          Background

          Sorghum ( Sorghum bicolor L.) is used as a raw material for biofuels because it accumulates sugars at high levels in the stem. Lodging of sorghum occurs when the soil is wet and very high winds blow across the field. In root lodging, the roots are pulled loose from the soil, causing the plant to fall over. Lodging reduces the yield of nonstructural carbohydrates. It is not yet clear which genes show changes in expression when sorghum falls over. We compared whole-gene expression in the mature stems of intact and lodged sorghum plants, with a focus on comparisons from the perspective of differences in sugar accumulation or degradation.

          Results

          Lodging decreased sucrose content, starch content, and ratio of sucrose to total sugars in the stems of the sorghum cultivar SIL-05. Particular paralogs of SWEET and TMT family genes, which encode sucrose or hexose transporters, or both, were significantly highly expressed in intact or lodged sorghum stems. In intact stems, genes encoding the glucose-6-phosphate translocator, aquaporins, and enzymes involved in photosynthesis and starch synthesis were highly expressed. In lodged sorghum stems, expression of genes associated with sucrose or starch degradation or energy production was increased. Notably, expression of genes encoding enzymes catalyzing irreversible reactions and associated with the first steps of these metabolic pathways (e.g. INV, SUS, and hexokinase- and fructokinase-encoding genes) was significantly increased by lodging. Expression of SUT, SPS, and SPP was almost the same in intact and lodged sorghum.

          Conclusions

          Specific paralogs of sucrose-associated genes involved in metabolic pathways and in membrane transport were expressed in the stems of sorghum SIL-05 at the full-ripe stage. Root lodging drastically changed the expression of these genes from sucrose accumulation to degradation. The changes in gene expression resulted in decreases in sugar content and in the proportion of sucrose to hexoses in the stems of lodged plants.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-017-1218-9) contains supplementary material, which is available to authorized users.

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          Most cited references19

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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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            Transport of sugars.

            Soluble sugars serve five main purposes in multicellular organisms: as sources of carbon skeletons, osmolytes, signals, and transient energy storage and as transport molecules. Most sugars are derived from photosynthetic organisms, particularly plants. In multicellular organisms, some cells specialize in providing sugars to other cells (e.g., intestinal and liver cells in animals, photosynthetic cells in plants), whereas others depend completely on an external supply (e.g., brain cells, roots and seeds). This cellular exchange of sugars requires transport proteins to mediate uptake or release from cells or subcellular compartments. Thus, not surprisingly, sugar transport is critical for plants, animals, and humans. At present, three classes of eukaryotic sugar transporters have been characterized, namely the glucose transporters (GLUTs), sodium-glucose symporters (SGLTs), and SWEETs. This review presents the history and state of the art of sugar transporter research, covering genetics, biochemistry, and physiology-from their identification and characterization to their structure, function, and physiology. In humans, understanding sugar transport has therapeutic importance (e.g., addressing diabetes or limiting access of cancer cells to sugars), and in plants, these transporters are critical for crop yield and pathogen susceptibility.
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              Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning.

              Brian Ayre (2011)
              Sucrose is the principal product of photosynthesis used for the distribution of assimilated carbon in plants. Transport mechanisms and efficiency influence photosynthetic productivity by relieving product inhibition and contribute to plant vigor by controlling source/sink relationships and biomass partitioning. Sucrose is synthesized in the cytoplasm and may move cell to cell through plasmodesmata or may cross membranes to be compartmentalized or exported to the apoplasm for uptake into adjacent cells. As a relatively large polar compound, sucrose requires proteins to facilitate efficient membrane transport. Transport across the tonoplast by facilitated diffusion, antiport with protons, and symport with protons have been proposed; for transport across plasma membranes, symport with protons and a mechanism resembling facilitated diffusion are evident. Despite decades of research, only symport with protons is well established at the molecular level. This review aims to integrate recent and older studies on sucrose flux across membranes with principles of whole-plant carbon partitioning.
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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
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                3 January 2018
                3 January 2018
                2018
                : 18
                : 2
                Affiliations
                [1 ]ISNI 0000 0001 2222 0432, GRID grid.416835.d, Institute of Crop Science (NICS), , National Agriculture and Food Research Organization, ; 2-1-2, Kannondai, Tsukuba, Ibaraki 305-8518 Japan
                [2 ]ISNI 0000 0001 1507 4692, GRID grid.263518.b, Faculty of Agriculture, , Shinshu University, ; 8304 Minami-minowa, Nagano, 399-4598 Japan
                Author information
                http://orcid.org/0000-0002-4110-4717
                Article
                1218
                10.1186/s12870-017-1218-9
                5751775
                29298675
                015dbd83-e0d2-4a45-bc37-b44bb5f4600b
                © The Author(s). 2018

                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
                : 8 August 2017
                : 19 December 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007172, National Agriculture and Food Research Organization;
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Plant science & Botany
                biofuel,rna-seq,stem,sugar content,sugar metabolism,sugar transporter
                Plant science & Botany
                biofuel, rna-seq, stem, sugar content, sugar metabolism, sugar transporter

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