Transcriptional regulation of the raffinose family oligosaccharides pathway in Sorghum bicolor reveals potential roles in leaf sucrose transport and stem sucrose accumulation

McKinley, Brian A.; Thakran, Manish; Zemelis-Durfee, Starla; Huang, Xinyi; Brandizzi, Federica; Rooney, William L.; Mansfield, Shawn D.; Mullet, John E.

doi:10.3389/fpls.2022.1062264

Transcriptional regulation of the raffinose family oligosaccharides pathway in Sorghum bicolor reveals potential roles in leaf sucrose transport and stem sucrose accumulation

Journal Article · Fri Dec 09 00:00:00 EST 2022 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2022.1062264· OSTI ID:1902777

McKinley, Brian A.; Thakran, Manish; Zemelis-Durfee, Starla; Huang, Xinyi; Brandizzi, Federica; Rooney, William L.; Mansfield, Shawn D.; Mullet, John E.

Bioenergy sorghum hybrids are being developed with enhanced drought tolerance and high levels of stem sugars. Raffinose family oligosaccharides (RFOs) contribute to plant environmental stress tolerance, sugar storage, transport, and signaling. To better understand the role of RFOs in sorghum, genes involved in myo -inositol and RFO metabolism were identified and relative transcript abundance analyzed during development. Genes involved in RFO biosynthesis ( SbMIPS1, SbInsPase, SbGolS1, SbRS ) were more highly expressed in leaves compared to stems and roots, with peak expression early in the morning in leaves. SbGolS, SbRS, SbAGA1 and SbAGA2 were also expressed at high levels in the leaf collar and leaf sheath. In leaf blades, genes involved in myo -inositol biosynthesis ( SbMIPS1, SbInsPase ) were expressed in bundle sheath cells, whereas genes involved in galactinol and raffinose synthesis ( SbGolS1, SbRS ) were expressed in mesophyll cells. Furthermore, SbAGA1 and SbAGA2 , genes that encode neutral-alkaline alpha-galactosidases that hydrolyze raffinose, were differentially expressed in minor vein bundle sheath cells and major vein and mid-rib vascular and xylem parenchyma. This suggests that raffinose synthesized from sucrose and galactinol in mesophyll cells diffuses into vascular bundles where hydrolysis releases sucrose for long distance phloem transport. Increased expression (>20-fold) of SbAGA1 and SbAGA2 in stem storage pith parenchyma of sweet sorghum between floral initiation and grain maturity, and higher expression in sweet sorghum compared to grain sorghum, indicates these genes may play a key role in non-structural carbohydrate accumulation in stems.

View Journal Article

Research Organization:: Univ. of California, Oakland, CA (United States); Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0018409

OSTI ID:: 1902777

Alternate ID(s):: OSTI ID: 2420810

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 13; ISSN 1664-462X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (83)

Designing sorghum as a dedicated bioenergy feedstock Rooney, William L.; Blumenthal, Jürg; Bean, Brent Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 2 https://doi.org/10.1002/bbb.15	journal	October 2007
A sorghum NAC gene is associated with variation in biomass properties and yield potential Xia, Jingnu; Zhao, Yunjun; Burks, Payne Plant Direct, Vol. 2, Issue 7 https://doi.org/10.1002/pld3.70	journal	July 2018
Developmental dynamics of stem starch accumulation in Sorghum bicolor McKinley, Brian A.; Casto, Anna L.; Rooney, William L. Plant Direct, Vol. 2, Issue 8 https://doi.org/10.1002/pld3.74	journal	August 2018
Sorghum stem aerenchyma formation is regulated by SbNAC_D during internode development Casto, Anna L.; McKinley, Brian A.; Yu, Ka Man Jasmine Plant Direct, Vol. 2, Issue 11 https://doi.org/10.1002/pld3.85	journal	November 2018
Leaf structure in relation to solute transport and phloem loading in Zea mays L. Evert, R. F.; Eschrich, W.; Heyser, W. Planta, Vol. 138, Issue 3 https://doi.org/10.1007/BF00386823	journal	January 1978
The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance Santarius, Kurt A. Planta, Vol. 113, Issue 2 https://doi.org/10.1007/BF00388196	journal	January 1973
Localisation of sucrose-phosphate synthase and starch in leaves of C 4 plants Furbank, Robert T.; Lunn, John E. Planta, Vol. 202, Issue 1 https://doi.org/10.1007/s004250050108	journal	April 1997
A novel alkaline α-galactosidase gene is involved in rice leaf senescence Lee, Ruey-Hua; Lin, Mei-Chung; Chen, Shu-Chen Plant Molecular Biology, Vol. 55, Issue 2 https://doi.org/10.1007/s11103-004-0641-0	journal	May 2004
Suppression of cucumber stachyose synthase gene (CsSTS) inhibits phloem loading and reduces low temperature stress tolerance Lü, Jianguo; Sui, Xiaolei; Ma, Si Plant Molecular Biology, Vol. 95, Issue 1-2 https://doi.org/10.1007/s11103-017-0621-9	journal	June 2017
Variability in crop radiation-use efficiency associated with vapor-pressure deficit Stockle, Claudio O.; Kiniry, James R. Field Crops Research, Vol. 25, Issue 3-4 https://doi.org/10.1016/0378-4290(90)90001-R	journal	December 1990
Current perspectives on the regulation of whole-plant carbohydrate partitioning Slewinski, Thomas L.; Braun, David M. Plant Science, Vol. 178, Issue 4 https://doi.org/10.1016/J.PLANTSCI.2010.01.010	journal	April 2010
myo-Inositol-1,2,3,4,5,6-hexakisphosphate Raboy, Victor Phytochemistry, Vol. 64, Issue 6 https://doi.org/10.1016/S0031-9422(03)00446-1	journal	November 2003
Techno-economic analysis of lignocellulosic ethanol: A review Gnansounou, Edgard; Dauriat, Arnaud Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2010.02.009	journal	July 2010
RNAscope Wang, Fay; Flanagan, John; Su, Nan The Journal of Molecular Diagnostics, Vol. 14, Issue 1 https://doi.org/10.1016/j.jmoldx.2011.08.002	journal	January 2012
Regulation of Seed Vigor by Manipulation of Raffinose Family Oligosaccharides in Maize and Arabidopsis thaliana Li, Tao; Zhang, Yumin; Wang, Dong Molecular Plant, Vol. 10, Issue 12 https://doi.org/10.1016/j.molp.2017.10.014	journal	December 2017
Starch turnover: pathways, regulation and role in growth Stitt, Mark; Zeeman, Samuel C. Current Opinion in Plant Biology, Vol. 15, Issue 3 https://doi.org/10.1016/j.pbi.2012.03.016	journal	June 2012
Myo-inositol and beyond – Emerging networks under stress Valluru, Ravi; Van den Ende, Wim Plant Science, Vol. 181, Issue 4 https://doi.org/10.1016/j.plantsci.2011.07.009	journal	October 2011
Galactinol as marker for seed longevity de Souza Vidigal, Deborah; Willems, Leo; van Arkel, Jeroen Plant Science, Vol. 246 https://doi.org/10.1016/j.plantsci.2016.02.015	journal	May 2016
Genetic variability of the phloem sap metabolite content of maize (Zea mays L.) during the kernel-filling period Yesbergenova-Cuny, Zhazira; Dinant, Sylvie; Martin-Magniette, Marie-Laure Plant Science, Vol. 252 https://doi.org/10.1016/j.plantsci.2016.08.007	journal	November 2016
High-biomass C 4 grasses—Filling the yield gap Mullet, John E. Plant Science, Vol. 261 https://doi.org/10.1016/j.plantsci.2017.05.003	journal	August 2017
Maize VIVIPAROUS1 Interacts with ABA INSENSITIVE5 to Regulate GALACTINOL SYNTHASE2 Expression Controlling Seed Raffinose Accumulation Zhang, Yumin; Sun, Qichao; Zhang, Chunxia Journal of Agricultural and Food Chemistry, Vol. 67, Issue 15 https://doi.org/10.1021/acs.jafc.9b00322	journal	March 2019
Sucrose accumulation in sweet sorghum stem internodes in relation to growth Hoffmann-Thoma, Gudrun; Hinkel, Karin; Nicolay, Peter Physiologia Plantarum, Vol. 97, Issue 2 https://doi.org/10.1034/j.1399-3054.1996.970210.x	journal	June 1996
Carbohydrate metabolism during early fruit development of sweet melon (Cucumis melo ) Gao, Zhifang; Petreikov, Marina; Zamski, Eli Physiologia Plantarum, Vol. 106, Issue 1 https://doi.org/10.1034/j.1399-3054.1999.106101.x	journal	May 1999
Dark-inducible genes from Arabidopsisthaliana are associated with leaf senescence and repressed by sugars Fujiki, Yuki; Yoshikawa, Yoko; Sato, Tokuyuki Physiologia Plantarum, Vol. 111, Issue 3 https://doi.org/10.1034/j.1399-3054.2001.1110312.x	journal	March 2001
A central integrator of transcription networks in plant stress and energy signalling Baena-González, Elena; Rolland, Filip; Thevelein, Johan M. Nature, Vol. 448, Issue 7156 https://doi.org/10.1038/nature06069	journal	August 2007
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M. Nature Biotechnology, Vol. 33, Issue 3 https://doi.org/10.1038/nbt.3122	journal	February 2015
HISAT: a fast spliced aligner with low memory requirements Kim, Daehwan; Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3317	journal	March 2015
Cloning and functional expression of alkaline alpha-galactosidase from melon fruit: similarity to plant SIP proteins uncovers a novel family of plant glycosyl hydrolases Carmi, Nir; Zhang, Genfa; Petreikov, Marina The Plant Journal, Vol. 33, Issue 1 https://doi.org/10.1046/j.1365-313X.2003.01609.x	journal	January 2003
Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga reptans: the roles of two distinct galactinol synthases Sprenger, Norbert; Keller, Felix The Plant Journal, Vol. 21, Issue 3 https://doi.org/10.1046/j.1365-313x.2000.00671.x	journal	February 2000
Grain, sugar and biomass accumulation in photoperiod-sensitive sorghums. II. Biochemical processes at internode level and interaction with phenology Gutjahr, Sylvain; Clément-Vidal, Anne; Soutiras, Armelle Functional Plant Biology, Vol. 40, Issue 4 https://doi.org/10.1071/FP12177	journal	January 2013
Grain, sugar and biomass accumulation in tropical sorghums. I. Trade-offs and effects of phenological plasticity Gutjahr, Sylvain; Vaksmann, Michel; Dingkuhn, Michaël Functional Plant Biology, Vol. 40, Issue 4 https://doi.org/10.1071/FP12269	journal	January 2013
Cellular pathways of source leaf phloem loading and phloem unloading in developing stems of Sorghum bicolor in relation to stem sucrose storage Milne, Ricky J.; Offler, Christina E.; Patrick, John W. Functional Plant Biology, Vol. 42, Issue 10 https://doi.org/10.1071/FP15133	journal	January 2015
Diurnal variation in gas exchange and nonstructural carbohydrates throughout sugarcane development De Souza, Amanda P.; Grandis, Adriana; Arenque-Musa, Bruna C. Functional Plant Biology, Vol. 45, Issue 8 https://doi.org/10.1071/FP17268	journal	January 2018
Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum Murphy, R. L.; Klein, R. R.; Morishige, D. T. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39, p. 16469-16474 https://doi.org/10.1073/Pnas.1106212108	journal	September 2011
Raffinose synthase enhances drought tolerance through raffinose synthesis or galactinol hydrolysis in maize and Arabidopsis plants Li, Tao; Zhang, Yumin; Liu, Ying Journal of Biological Chemistry, Vol. 295, Issue 23 https://doi.org/10.1074/jbc.RA120.013948	journal	June 2020
An alkaline α-galactosidase transcript is present in maize seeds and cultured embryo cells, and accumulates during stress Zhao, Tian-Yong; Corum III, J. Willis; Mullen, Jeffrey Seed Science Research, Vol. 16, Issue 2 https://doi.org/10.1079/SSR2006243	journal	June 2006
Tonoplast Sugar Transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems Bihmidine, Saadia; Julius, Benjamin T.; Dweikat, Ismail Plant Signaling & Behavior, Vol. 11, Issue 1 https://doi.org/10.1080/15592324.2015.1117721	journal	January 2016
The rapid generation of mutation data matrices from protein sequences Jones, David T.; Taylor, William R.; Thornton, Janet M. Bioinformatics, Vol. 8, Issue 3 https://doi.org/10.1093/bioinformatics/8.3.275	journal	January 1992
Sink regulation of photosynthesis Paul, Matthew J.; Foyer, Christine H. Journal of Experimental Botany, Vol. 52, Issue 360 https://doi.org/10.1093/jexbot/52.360.1383	journal	July 2001
Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit Peters, S.; Mundree, S. G.; Thomson, J. A. Journal of Experimental Botany, Vol. 58, Issue 8 https://doi.org/10.1093/jxb/erm056	journal	April 2007
Sucrose transporter1 functions in phloem loading in maize leaves Slewinski, Thomas L.; Meeley, Robert; Braun, David M. Journal of Experimental Botany, Vol. 60, Issue 3 https://doi.org/10.1093/jxb/ern335	journal	January 2009
Evidence for functional heterogeneity of sieve element–companion cell complexes in minor vein phloem of Alonsoa meridionalis Voitsekhovskaja, Olga V.; Rudashevskaya, Elena L.; Demchenko, Kirill N. Journal of Experimental Botany, Vol. 60, Issue 6 https://doi.org/10.1093/jxb/erp074	journal	March 2009
Energy Sorghum--a genetic model for the design of C4 grass bioenergy crops Mullet, J.; Morishige, D.; McCormick, R. Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru229	journal	June 2014
MEGA11: Molecular Evolutionary Genetics Analysis Version 11 Tamura, Koichiro; Stecher, Glen; Kumar, Sudhir Molecular Biology and Evolution, Vol. 38, Issue 7 https://doi.org/10.1093/molbev/msab120	journal	April 2021
Molecular Evolutionary Genetics Analysis (MEGA) for macOS Stecher, Glen; Tamura, Koichiro; Kumar, Sudhir Molecular Biology and Evolution, Vol. 37, Issue 4 https://doi.org/10.1093/molbev/msz312	journal	January 2020
Increased coverage of protein families with the Blocks Database servers Henikoff, J. G. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.228	journal	January 2000
Changes in the Sugarcane Metabolome with Stem Development. Are They Related to Sucrose Accumulation? Glassop, Donna; Roessner, Ute; Bacic, Antony Plant and Cell Physiology, Vol. 48, Issue 4 https://doi.org/10.1093/pcp/pcm027	journal	April 2007
Raffinose in Chloroplasts is Synthesized in the Cytosol and Transported across the Chloroplast Envelope Schneider, T.; Keller, F. Plant and Cell Physiology, Vol. 50, Issue 12 https://doi.org/10.1093/pcp/pcp151	journal	October 2009
Functional Identification of Arabidopsis ATSIP2 (At3g57520) as an Alkaline -Galactosidase with a Substrate Specificity for Raffinose and an Apparent Sink-Specific Expression Pattern Peters, S.; Egert, A.; Stieger, B. Plant and Cell Physiology, Vol. 51, Issue 10 https://doi.org/10.1093/pcp/pcq127	journal	August 2010
Differences in growth and physiological and metabolic responses among Canadian native and hybrid willows (Salix spp.) under salinity stress Huang, Xinyi; Soolanayakanahally, Raju Y.; Guy, Robert D. Tree Physiology, Vol. 40, Issue 5 https://doi.org/10.1093/treephys/tpaa017	journal	February 2020
Sucrose phosphate synthase expression influences poplar phenology Park, J. -Y.; Canam, T.; Kang, K. -Y. Tree Physiology, Vol. 29, Issue 7 https://doi.org/10.1093/treephys/tpp028	journal	May 2009
Galactinol and Raffinose Constitute a Novel Function to Protect Plants from Oxidative Damage Nishizawa, Ayako; Yabuta, Yukinori; Shigeoka, Shigeru Plant Physiology, Vol. 147, Issue 3 https://doi.org/10.1104/pp.108.122465	journal	May 2008
Studies ofaberrant phyllotaxy1Mutants of Maize Indicate Complex Interactions between Auxin and Cytokinin Signaling in the Shoot Apical Meristem Lee, Byeong-ha; Johnston, Robyn; Yang, Yan Plant Physiology, Vol. 150, Issue 1 https://doi.org/10.1104/pp.109.137034	journal	March 2009
Metabolism of the Raffinose Family Oligosaccharides in Leaves of Ajuga reptans L. (Inter- and Intracellular Compartmentation) Bachmann, M.; Keller, F. Plant Physiology, Vol. 109, Issue 3 https://doi.org/10.1104/pp.109.3.991	journal	November 1995
Sucrose Transporter ZmSut1 Expression and Localization Uncover New Insights into Sucrose Phloem Loading Baker, R. Frank; Leach, Kristen A.; Boyer, Nathanial R. Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.00884	journal	September 2016
Sucrose Transporter Localization and Function in Phloem Unloading in Developing Stems Milne, Ricky J.; Perroux, Jai M.; Rae, Anne L. Plant Physiology, Vol. 173, Issue 2 https://doi.org/10.1104/pp.16.01594	journal	December 2016
Bioenergy sorghum’s deep roots: A key to sustainable biomass production on annual cropland Lamb, Austin; Weers, Brock; McKinley, Brian GCB Bioenergy, Vol. 14, Issue 2 https://doi.org/10.1111/gcbb.12907	journal	December 2021
Sieve element unloading: cellular pathway, mechanism and control Patrick, J. W. Physiologia Plantarum, Vol. 78, Issue 2 https://doi.org/10.1111/j.1399-3054.1990.tb02095.x	journal	February 1990
Alkaline α‐galactosidase degrades thylakoid membranes in the chloroplast during leaf senescence in rice Lee, Ruey‐Hua; Hsu, Jen‐Hung; Huang, Hao‐Jen New Phytologist, Vol. 184, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.02999.x	journal	October 2009
Sugar signalling and antioxidant network connections in plant cells Bolouri-Moghaddam, Mohammad Reza; Le Roy, Katrien; Xiang, Li FEBS Journal, Vol. 277, Issue 9 https://doi.org/10.1111/j.1742-4658.2010.07633.x	journal	April 2010
C4 Plants as Biofuel Feedstocks: Optimising Biomass Production and Feedstock Quality from a Lignocellulosic PerspectiveFree Access Byrt, Caitlin S.; Grof, Christopher P. L.; Furbank, Robert T. Journal of Integrative Plant Biology, Vol. 53, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.01023.x	journal	January 2011
Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays Bezrutczyk, Margaret; Hartwig, Thomas; Horschman, Marc New Phytologist, Vol. 218, Issue 2 https://doi.org/10.1111/nph.15021	journal	February 2018
Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development Unda, Faride; Kim, Hoon; Hefer, Charles Plant Biotechnology Journal, Vol. 15, Issue 7 https://doi.org/10.1111/pbi.12682	journal	March 2017
Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes Li, Yin; Wang, Wenqin; Feng, Yaping Plant Biotechnology Journal, Vol. 17, Issue 2 https://doi.org/10.1111/pbi.12991	journal	September 2018
Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress ElSayed, A. I.; Rafudeen, M. S.; Golldack, D. Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1111/plb.12053	journal	August 2013
Dynamics of biomass partitioning, stem gene expression, cell wall biosynthesis, and sucrose accumulation during development of Sorghum bicolor McKinley, Brian; Rooney, William; Wilkerson, Curtis The Plant Journal, Vol. 88, Issue 4 https://doi.org/10.1111/tpj.13269	journal	September 2016
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash The Plant Journal, Vol. 93, Issue 2 https://doi.org/10.1111/tpj.13781	journal	December 2017
Phloem loading in cucumber: combined symplastic and apoplastic strategies Ma, Si; Sun, Lulu; Sui, Xiaolei The Plant Journal, Vol. 98, Issue 3 https://doi.org/10.1111/tpj.14224	journal	February 2019
Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport Chen, L. -Q.; Qu, X. -Q.; Hou, B. -H. Science, Vol. 335, Issue 6065 https://doi.org/10.1126/science.1213351	journal	December 2011
Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development Covington, Michael F.; Maloof, Julin N.; Straume, Marty Genome Biology, Vol. 9, Issue 8 https://doi.org/10.1186/gb-2008-9-8-r130	journal	January 2008
Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression Bihmidine, Saadia; Baker, R. Frank; Hoffner, Cassandra BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0572-8	journal	July 2015
Visualization of spatial gene expression in plants by modified RNAscope fluorescent in situ hybridization Solanki, Shyam; Ameen, Gazala; Zhao, Jin Plant Methods, Vol. 16, Issue 1 https://doi.org/10.1186/s13007-020-00614-4	journal	May 2020
Harnessing Genetic Variation in Leaf Angle to Increase Productivity of Sorghum bicolor Truong, Sandra K.; McCormick, Ryan F.; Rooney, William L. Genetics, Vol. 201, Issue 3 https://doi.org/10.1534/genetics.115.178608	journal	August 2015
Sucrose Metabolism in the Primary Culm of Sweet Sorghum During Development1 Lingle, Sarah E. Crop Science, Vol. 27, Issue 6 https://doi.org/10.2135/cropsci1987.0011183X002700060025x	journal	January 1987
Genetic Improvement of Sorghum as a Biofuel Feedstock: I. QTL for Stem Sugar and Grain Nonstructural Carbohydrates Murray, Seth C.; Sharma, Arun; Rooney, William L. Crop Science, Vol. 48, Issue 6 https://doi.org/10.2135/cropsci2008.01.0016	journal	January 2008
Regulation of assimilate import into sink organs: update on molecular drivers of sink strength Bihmidine, Saadia; Hunter, Charles T.; Johns, Christine E. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00177	journal	January 2013
Structural and functional heterogeneity in phloem loading and transport Slewinski, Thomas L.; Zhang, Cankui; Turgeon, Robert Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00244	journal	January 2013
A tale of two neglected systems—structure and function of the thin- and thick-walled sieve tubes in monocotyledonous leaves Botha, C. E. J. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00297	journal	January 2013
Significance of galactinol and raffinose family oligosaccharide synthesis in plants Sengupta, Sonali; Mukherjee, Sritama; Basak, Papri Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00656	journal	August 2015
Molecular cloning of AtRS4, a seed specific multifunctional RFO synthase/galactosylhydrolase in Arabidopsis thaliana Gangl, Roman; Behmüller, Robert; Tenhaken, Raimund Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00789	journal	September 2015
Raffinose Family Oligosaccharides Act As Galactose Stores in Seeds and Are Required for Rapid Germination of Arabidopsis in the Dark Gangl, Roman; Tenhaken, Raimund Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01115	journal	July 2016
Non-radioactive in situ Hybridization Protocol Applicable for Norway Spruce and a Range of Plant Species Karlgren, Anna; Carlsson, Jenny; Gyllenstrand, Niclas Journal of Visualized Experiments, Issue 26 https://doi.org/10.3791/1205	journal	January 2009
The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage Nishizawa-Yokoi, Ayako; Yabuta, Yukinori; Shigeoka, Shigeru Plant Signaling & Behavior, Vol. 3, Issue 11 https://doi.org/10.4161/psb.6738	journal	November 2008

Similar Records

Altering carbon allocation in hybrid poplar ( Populus alba × grandidentata ) impacts cell wall growth and development

Journal Article · Fri Mar 03 19:00:00 EST 2017 · Plant Biotechnology Journal · OSTI ID:1374538

Related Subjects

60 APPLIED LIFE SCIENCES
Plant Sciences
bioenergy sorghum
inositol
phloem loading
raffinose
sugar transport

Transcriptional regulation of the raffinose family oligosaccharides pathway in Sorghum bicolor reveals potential roles in leaf sucrose transport and stem sucrose accumulation

Citation Formats

References (83)

Similar Records

Related Subjects