SWEET 11 and 15 as key players in seed filling in rice
Abstract
Despite the relevance of seed-filling mechanisms for crop yield, we still have only a rudimentary understanding of the transport processes that supply the caryopsis with sugars. Here, we hypothesized that SWEET sucrose transporters may play important roles in nutrient import pathways in the rice caryopsis. We used a combination of mRNA quantification, histochemical analyses, translational promoter–reporter fusions and analysis of knockout mutants created by genomic editing to evaluate the contribution of SWEET transporters to seed filling. In rice caryopses, SWEET11 and 15 had the highest mRNA levels and proteins localized to four key sites: all regions of the nucellus at early stages; the nucellar projection close to the dorsal vein; the nucellar epidermis that surrounds the endosperm; and the aleurone. ossweet11;15 double knockout lines accumulated starch in the pericarp, whereas caryopses did not contain a functional endosperm. Jointly, SWEET11 and 15 show all the hallmarks of being necessary for seed filling with sucrose efflux functions at the nucellar projection and a role in transfer across the nucellar epidermis/aleurone interface, delineating two major steps for apoplasmic seed filling, observations that are discussed in relation to observations made in rice and barley regarding the relative prevalence of these two potential import routes.
- Authors:
-
- Institute for Molecular Physiology Heinrich‐Heine University Duesseldorf 40225 Duesseldorf Germany, Max Planck Institute for Plant Breeding Research 50829 Cologne Germany, Department of Plant Biology Carnegie Institution for Science Stanford CA 94305 USA
- Department of Genetics, Development, and Cell Biology Iowa State University Ames IA 50011 USA
- Institute for Molecular Physiology Heinrich‐Heine University Duesseldorf 40225 Duesseldorf Germany, Max Planck Institute for Plant Breeding Research 50829 Cologne Germany, Department of Plant Biology Carnegie Institution for Science Stanford CA 94305 USA, Institute of Transformative Bio‐Molecules (ITbM) Nagoya University Furo‐cho, Chikusa‐ku Nagoya Aichi 464‐8602 Japan
- Publication Date:
- Research Org.:
- Carnegie Inst. of Washington, Washington, DC (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1419360
- Alternate Identifier(s):
- OSTI ID: 1419361; OSTI ID: 1500104
- Grant/Contract Number:
- DE‐FG02‐04ER15542; FG02-04ER15542
- Resource Type:
- Published Article
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 218 Journal Issue: 2; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; apoplasmic pathway; caryopsis; endosperm; rice; sucrose transporter; SWEET
Citation Formats
Yang, Jungil, Luo, Dangping, Yang, Bing, Frommer, Wolf B., and Eom, Joon‐Seob. SWEET 11 and 15 as key players in seed filling in rice. United Kingdom: N. p., 2018.
Web. doi:10.1111/nph.15004.
Yang, Jungil, Luo, Dangping, Yang, Bing, Frommer, Wolf B., & Eom, Joon‐Seob. SWEET 11 and 15 as key players in seed filling in rice. United Kingdom. https://doi.org/10.1111/nph.15004
Yang, Jungil, Luo, Dangping, Yang, Bing, Frommer, Wolf B., and Eom, Joon‐Seob. Fri .
"SWEET 11 and 15 as key players in seed filling in rice". United Kingdom. https://doi.org/10.1111/nph.15004.
@article{osti_1419360,
title = {SWEET 11 and 15 as key players in seed filling in rice},
author = {Yang, Jungil and Luo, Dangping and Yang, Bing and Frommer, Wolf B. and Eom, Joon‐Seob},
abstractNote = {Despite the relevance of seed-filling mechanisms for crop yield, we still have only a rudimentary understanding of the transport processes that supply the caryopsis with sugars. Here, we hypothesized that SWEET sucrose transporters may play important roles in nutrient import pathways in the rice caryopsis. We used a combination of mRNA quantification, histochemical analyses, translational promoter–reporter fusions and analysis of knockout mutants created by genomic editing to evaluate the contribution of SWEET transporters to seed filling. In rice caryopses, SWEET11 and 15 had the highest mRNA levels and proteins localized to four key sites: all regions of the nucellus at early stages; the nucellar projection close to the dorsal vein; the nucellar epidermis that surrounds the endosperm; and the aleurone. ossweet11;15 double knockout lines accumulated starch in the pericarp, whereas caryopses did not contain a functional endosperm. Jointly, SWEET11 and 15 show all the hallmarks of being necessary for seed filling with sucrose efflux functions at the nucellar projection and a role in transfer across the nucellar epidermis/aleurone interface, delineating two major steps for apoplasmic seed filling, observations that are discussed in relation to observations made in rice and barley regarding the relative prevalence of these two potential import routes.},
doi = {10.1111/nph.15004},
journal = {New Phytologist},
number = 2,
volume = 218,
place = {United Kingdom},
year = {2018},
month = {2}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/nph.15004
https://doi.org/10.1111/nph.15004
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 137 works
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
Fig. 1: Relative expression of OsSWEET4, OsSWEET11 and OsSWEET15 during rice seed development after pollination. Expression was measured by quantitative reverse transcription polymerase chain reaction (qRT-PCR) in wild-type glasshouse-grown seeds. Data shown as mean ± SEM, n = 3; expression levels were normalized to rice Ubiquitin1 levels.
All figures and tables
(7 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Spatiotemporal Profiling of Starch Biosynthesis and Degradation in the Developing Barley Grain
journal, March 2009
- Radchuk, Volodymyr V.; Borisjuk, Ludmilla; Sreenivasulu, Nese
- Plant Physiology, Vol. 150, Issue 1
Microarray Analysis of Sink-Source Transition in Rice Leaf Sheaths
journal, January 2005
- Takahashi, Sakiko; Ishimaru, Ken; Yazaki, Junshi
- Breeding Science, Vol. 55, Issue 2
Sugar Absorption in the Intestine: The Role of GLUT2
journal, August 2008
- Kellett, George L.; Brot-Laroche, Edith; Mace, Oliver J.
- Annual Review of Nutrition, Vol. 28, Issue 1
Sucrose transporter1 functions in phloem loading in maize leaves
journal, January 2009
- Slewinski, Thomas L.; Meeley, Robert; Braun, David M.
- Journal of Experimental Botany, Vol. 60, Issue 3
Functional role of oligomerization for bacterial and plant SWEET sugar transporter family
journal, September 2013
- Xuan, Y. H.; Hu, Y. B.; Chen, L. -Q.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 39
Ultrastructure of the developing pigment strand of rice (Oryza sativa L.) in relation to its role in solute transport
journal, February 1982
- Oparka, K. J.; Gates, P. J.
- Protoplasma, Vol. 113, Issue 1
The Bacterial Pathogen Xanthomonas oryzae Overcomes Rice Defenses by Regulating Host Copper Redistribution
journal, September 2010
- Yuan, Meng; Chu, Zhaohui; Li, Xianghua
- The Plant Cell, Vol. 22, Issue 9
Transport of assimilates in the developing caryopsis of rice (Oryza sativa L.): Ultrastructure of the pericarp vascular bundle and its connections with the aleurone layer
journal, May 1981
- Oparka, K. J.; Gates, P.
- Planta, Vol. 151, Issue 6
Control of rice grain-filling and yield by a gene with a potential signature of domestication
journal, September 2008
- Wang, Ertao; Wang, Jianjun; Zhu, Xudong
- Nature Genetics, Vol. 40, Issue 11
Cellular localisation and function of a sucrose transporter OsSUT1 in developing rice grains
journal, January 2001
- Furbank, Robert T.; Scofield, Graham N.; Hirose, Tatsuro
- Functional Plant Biology, Vol. 28, Issue 12
Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays
journal, February 2018
- Bezrutczyk, Margaret; Hartwig, Thomas; Horschman, Marc
- New Phytologist, Vol. 218, Issue 2
The Sucrose Transporter Gene Family in Rice
journal, March 2003
- Aoki, Naohiro; Hirose, Tatsuro; Scofield, Graham N.
- Plant and Cell Physiology, Vol. 44, Issue 3
Rice caryopsis development I: Dynamic changes in different cell layers: Rice caryopsis development I
journal, December 2015
- Wu, Xiaoba; Liu, Jinxin; Li, Dongqi
- Journal of Integrative Plant Biology, Vol. 58, Issue 9
Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected
journal, July 2010
- Hirose, Tatsuro; Zhang, Zujian; Miyao, Akio
- Journal of Experimental Botany, Vol. 61, Issue 13
The mechanism of phloem loading in rice (Oryza sativa)
journal, March 2012
- Eom, Joon-Seob; Choi, Sang-Bong; Ward, John M.
- Molecules and Cells, Vol. 33, Issue 5
TALEN utilization in rice genome modifications
journal, August 2014
- Li, Ting; Liu, Bo; Chen, Chih Ying
- Methods, Vol. 69, Issue 1
Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport
journal, December 2011
- Chen, L. -Q.; Qu, X. -Q.; Hou, B. -H.
- Science, Vol. 335, Issue 6065
Characterization and Expression of Monosaccharide Transporters (OsMSTs) in Rice
journal, August 2000
- Toyofuku, Kyoko; Kasahara, Michihiro; Yamaguchi, Junji
- Plant and Cell Physiology, Vol. 41, Issue 8
Molecular Physiology of Legume seed Development
journal, June 2005
- Weber, Hans; Borisjuk, Ljudmilla; Wobus, Ulrich
- Annual Review of Plant Biology, Vol. 56, Issue 1
Rice caryopsis development II: Dynamic changes in the endosperm: Rice caryopsis development-endosperm II
journal, September 2016
- Wu, Xiaoba; Liu, Jinxin; Li, Dongqi
- Journal of Integrative Plant Biology, Vol. 58, Issue 9
The Monosaccharide Transporter Gene Family in Arabidopsis and Rice: A History of Duplications, Adaptive Evolution, and Functional Divergence
journal, September 2007
- Johnson, Deborah A.; Thomas, Michael A.
- Molecular Biology and Evolution, Vol. 24, Issue 11
Molecular cloning, functional characterization and expression analysis of a novel monosaccharide transporter gene OsMST6 from rice (Oryza sativa L.)
journal, May 2008
- Wang, Yongqin; Xiao, Yuguo; Zhang, Yu
- Planta, Vol. 228, Issue 4
NF-YB1-regulated expression of sucrose transporters in aleurone facilitates sugar loading to rice endosperm
journal, September 2015
- Bai, Ai-Ning; Lu, Xiao-Duo; Li, Dong-Qi
- Cell Research, Vol. 26, Issue 3
Structural and physiological characterization during wheat pericarp development
journal, April 2013
- Xiong, F.; Yu, X. R.; Zhou, L.
- Plant Cell Reports, Vol. 32, Issue 8
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Dynamic Proteomic Analysis Reveals a Switch between Central Carbon Metabolism and Alcoholic Fermentation in Rice Filling Grains
journal, August 2008
- Xu, Sheng Bao; Li, Tang; Deng, Zhu Yun
- Plant Physiology, Vol. 148, Issue 2
Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice
journal, September 2014
- Zhou, Huanbin; Liu, Bo; Weeks, Donald P.
- Nucleic Acids Research, Vol. 42, Issue 17
Sugar transporters for intercellular exchange and nutrition of pathogens
journal, November 2010
- Chen, Li-Qing; Hou, Bi-Huei; Lalonde, Sylvie
- Nature, Vol. 468, Issue 7323
PHLOEM UNLOADING: Sieve Element Unloading and Post-Sieve Element Transport
journal, June 1997
- Patrick, J. W.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 48, Issue 1
Rice xa13 Recessive Resistance to Bacterial Blight Is Defeated by Induction of the Disease Susceptibility Gene Os- 11N3
journal, November 2010
- Antony, Ginny; Zhou, Junhui; Huang, Sheng
- The Plant Cell, Vol. 22, Issue 11
Mechanism of Substrate Translocation in an Alternating Access Transporter
journal, March 2017
- Latorraca, Naomi R.; Fastman, Nathan M.; Venkatakrishnan, A. J.
- Cell, Vol. 169, Issue 1
Molecular mechanism of substrate recognition and transport by the AtSWEET13 sugar transporter
journal, September 2017
- Han, Lei; Zhu, Yongping; Liu, Min
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 38
Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis
journal, January 2002
- Scofield, Graham N.; Hirose, Tatsuro; Gaudron, Judy A.
- Functional Plant Biology, Vol. 29, Issue 7
A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators: Novel sucrose transporters expressed in legume seed coats
journal, January 2007
- Zhou, Yuchan; Qu, Hongxia; Dibley, Katherine E.
- The Plant Journal, Vol. 49, Issue 4
The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants
journal, December 2006
- Scofield, G. N.; Aoki, N.; Hirose, T.
- Journal of Experimental Botany, Vol. 58, Issue 3
Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport
journal, November 2015
- Sosso, Davide; Luo, Dangping; Li, Qin-Bao
- Nature Genetics, Vol. 47, Issue 12
Structure and function of SemiSWEET and SWEET sugar transporters
journal, August 2015
- Feng, Liang; Frommer, Wolf B.
- Trends in Biochemical Sciences, Vol. 40, Issue 8
Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.)
journal, June 2003
- Krishnan, S.; Dayanandan, P.
- Journal of Biosciences, Vol. 28, Issue 4
Essential Role of Sugar Transporter OsSWEET11 During the Early Stage of Rice Grain Filling
journal, March 2017
- Ma, Lai; Zhang, Dechun; Miao, Qisong
- Plant and Cell Physiology, Vol. 58, Issue 5
Transport of assimilates in the developing caryopsis of rice (Oryza sativa L.): The pathways of water and assimilated carbon
journal, August 1981
- Oparka, K. J.; Gates, P.
- Planta, Vol. 152, Issue 5
Os8N3 is a host disease-susceptibility gene for bacterial blight of rice
journal, June 2006
- Yang, B.; Sugio, A.; White, F. F.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
Compartmentation of transport and transfer events in developing seeds
journal, April 2001
- Patrick, John W.; Offler, Christina E.
- Journal of Experimental Botany, Vol. 52, Issue 356
Dynamic 13C/1H NMR imaging uncovers sugar allocation in the living seed: Sucrose allocation in seed
journal, April 2011
- Melkus, Gerd; Rolletschek, Hardy; Fuchs, Johannes
- Plant Biotechnology Journal, Vol. 9, Issue 9
Sink anatomy in relation to solute movement in rice (Oryza sativa L.): A summary of findings
journal, January 1984
- Oparka, K. J.; Gates, P.
- Plant Growth Regulation, Vol. 2, Issue 4
cDNA Cloning and Tissue Specific Expression of a Gene for Sucrose Transporter from Rice (Oryza sativa L.)
journal, January 1997
- Hirose, T.; Imaizumi, N.; Scofield, G. N.
- Plant and Cell Physiology, Vol. 38, Issue 12
Review: Nutrient loading of developing seeds
journal, January 2007
- Zhang, Wen-Hao; Zhou, Yuchan; Dibley, Katherine E.
- Functional Plant Biology, Vol. 34, Issue 4
Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice
journal, July 2007
- Scofield, G. N.; Hirose, T.; Aoki, N.
- Journal of Experimental Botany, Vol. 58, Issue 12
Mechanism of glucose and maltose transport in plasma-membrane vesicles from the yeast Candida utilis
journal, January 1997
- Broek, Peter J. A. van den; Gompel, Angeline E. van; Luttik, Marijke A. H.
- Biochemical Journal, Vol. 321, Issue 2
High-efficiency TALEN-based gene editing produces disease-resistant rice
journal, May 2012
- Li, Ting; Liu, Bo; Spalding, Martin H.
- Nature Biotechnology, Vol. 30, Issue 5
Transport of Sugars
journal, June 2015
- Chen, Li-Qing; Cheung, Lily S.; Feng, Liang
- Annual Review of Biochemistry, Vol. 84, Issue 1
Genetic evidence that invertase-mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize
journal, March 1999
- Cheng, Wan-Hsing; Chourey, Prem S.
- Theoretical and Applied Genetics, Vol. 98, Issue 3-4
A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo
journal, March 2015
- Chen, Li-Qing; Lin, I. Winnie; Qu, Xiao-Qing
- The Plant Cell, Vol. 27, Issue 3
Cell Wall Invertase in Developing Rice Caryopsis: Molecular Cloning of OsCIN1 and Analysis of its Expression in Relation to its Role in Grain Filling
journal, April 2002
- Hirose, Tatsuro; Takano, Makoto; Terao, Tomio
- Plant and Cell Physiology, Vol. 43, Issue 4
Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9
journal, March 2014
- Lin, I. Winnie; Sosso, Davide; Chen, Li-Qing
- Nature, Vol. 508, Issue 7497
Molecular cloning and expression analysis of a monosaccharide transporter gene OsMST4 from rice (Oryza sativa L.)
journal, September 2007
- Wang, Yongqin; Xu, Honglin; Wei, Xiaoli
- Plant Molecular Biology, Vol. 65, Issue 4
Identification of Amino Acids Important for Substrate Specificity in Sucrose Transporters Using Gene Shuffling
journal, July 2012
- Reinders, Anke; Sun, Ye; Karvonen, Kayla L.
- Journal of Biological Chemistry, Vol. 287, Issue 36
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.