Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance

Zhang, Jin; Li, Yu; Liu, Bobin; Wang, Lijuan; Zhang, Li; Hu, Jianjun; Chen, Jun; Zheng, Huanquan; Lu, Mengzhu

doi:10.1186/s12870-018-1342-1

Title: Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance

Journal Article · Mon Jun 18 00:00:00 EDT 2018 · BMC Plant Biology

DOI:https://doi.org/10.1186/s12870-018-1342-1· OSTI ID:1626849

^[1]; Li, Yu ^[2]; Liu, Bobin ^[2]; Wang, Lijuan ^[2]; Zhang, Li ^[2]; Hu, Jianjun ^[2]; Chen, Jun ^[2]; Zheng, Huanquan ^[3]; Lu, Mengzhu ^[2]

Chinese Academy of Forestry, Beijing (China); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Chinese Academy of Forestry, Beijing (China)
McGill Univ., Montreal, QC (Canada)

Background: Rab proteins form the largest family of the Ras superfamily of small GTP-binding proteins and regulate intracellular trafficking pathways. However, the function of the Rab proteins in woody species is still an open question. Results: Here, a total of 67 PtRabs were identified in Populus trichocarpa and categorized into eight subfamilies (RabA-RabH). Based on their chromosomal distribution and duplication blocks in the Populus genome, a total of 27 PtRab paralogous pairs were identified and all of them were generated by whole-genome duplication events. Combined the expression correlation and duplication date, the PtRab paralogous pairs that still keeping highly similar expression patterns were generated around the latest large-scale duplication (~ 13 MYA). The cis-elements and co-expression network of unique expanded PtRabs suggest their potential roles in poplar development and environmental responses. Subcellular localization of PtRabs from each subfamily indicates each subfamily shows a localization pattern similar to what is revealed in Arabidopsis but RabC shows a localization different from their counterparts. Furthermore, we characterized PtRabE1b by overexpressing its constitutively active mutant PtRabE1b(Q74L) in poplar and found that PtRabE1b(Q74L) enhanced the salt tolerance. Conclusions: These findings provide new insights into the functional divergence of PtRabs and resources for genetic engineering resistant breeding in tree species.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division; National Natural Science Foundation of China (NSFC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1626849

Journal Information:: BMC Plant Biology, Vol. 18, Issue 1; ISSN 1471-2229

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Membrane Traffic Within the Golgi Apparatus Glick, Benjamin S.; Nakano, Akihiko Annual Review of Cell and Developmental Biology, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.cellbio.24.110707.175421	journal	November 2009
Chrysanthemum CmHSFA4 gene positively regulates salt stress tolerance in transgenic chrysanthemum Li, Fei; Zhang, Huanru; Zhao, Husheng Plant Biotechnology Journal, Vol. 16, Issue 7 https://doi.org/10.1111/pbi.12871	journal	January 2018
The Arabidopsis Rab GTPase family: another enigma variation Rutherford, Stephen; Moore, Ian Current Opinion in Plant Biology, Vol. 5, Issue 6 https://doi.org/10.1016/S1369-5266(02)00307-2	journal	December 2002
The Rab GTPase RabG3b Positively Regulates Autophagy and Immunity-Associated Hypersensitive Cell Death in Arabidopsis Kwon, Soon Il; Cho, Hong Joo; Kim, Sung Ryul Plant Physiology, Vol. 161, Issue 4 https://doi.org/10.1104/pp.112.208108	journal	February 2013
The role of Rab GTPases in cell wall metabolism Lycett, G. Journal of Experimental Botany, Vol. 59, Issue 15 https://doi.org/10.1093/jxb/ern255	journal	October 2008
Diversification of the RAB Guanosine Triphosphatase Family in Dicots and Monocots Zhang, Jiaming; Hill, Daniel R.; Sylvester, Anne W. Journal of Integrative Plant Biology, Vol. 49, Issue 8 https://doi.org/10.1111/j.1672-9072.2007.00520.x	journal	August 2007
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
Overexpression of constitutively active Arabidopsis RabG3b promotes xylem development in transgenic poplars: RabG3b and xylem development in poplar Kwon, Soon Il; Cho, Hong Joo; Lee, Jae-Soon Plant, Cell & Environment, Vol. 34, Issue 12 https://doi.org/10.1111/j.1365-3040.2011.02416.x	journal	September 2011
The Ka/Ks ratio: diagnosing the form of sequence evolution Hurst, Laurence D. Trends in Genetics, Vol. 18, Issue 9 https://doi.org/10.1016/S0168-9525(02)02722-1	journal	September 2002
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Plant molecular stress responses face climate change Ahuja, Ishita; de Vos, Ric C. H.; Bones, Atle M. Trends in Plant Science, Vol. 15, Issue 12 https://doi.org/10.1016/j.tplants.2010.08.002	journal	December 2010
The Mechanisms of Vesicle Budding and Fusion Bonifacino, Juan S.; Glick, Benjamin S. Cell, Vol. 116, Issue 2 https://doi.org/10.1016/S0092-8674(03)01079-1	journal	January 2004
Pausing of Golgi Bodies on Microtubules Regulates Secretion of Cellulose Synthase Complexes in Arabidopsis Crowell, E. F.; Bischoff, V.; Desprez, T. The Plant Cell, Vol. 21, Issue 4, p. 1141-1154 https://doi.org/10.1105/tpc.108.065334	journal	April 2009
A brief history of hemoglobins: plant, animal, protist, and bacteria. Hardison, R. C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 12 https://doi.org/10.1073/pnas.93.12.5675	journal	June 1996
Subclass-specific sequence motifs identified in Rab GTPases Moore, Ian; Schell, Jeff; Palme, Klaus Trends in Biochemical Sciences, Vol. 20, Issue 1 https://doi.org/10.1016/S0968-0004(00)88939-2	journal	January 1995
AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato Bogdanove, A. J.; Martin, G. B. Proceedings of the National Academy of Sciences, Vol. 97, Issue 16 https://doi.org/10.1073/pnas.97.16.8836	journal	August 2000
Over-expression of a Rab family GTPase from phreatophyte Prosopis juliflora confers tolerance to salt stress on transgenic tobacco George, Suja; Parida, Ajay Molecular Biology Reports, Vol. 38, Issue 3 https://doi.org/10.1007/s11033-010-0278-9	journal	September 2010
GSDS 2.0: an upgraded gene feature visualization server Hu, Bo; Jin, Jinpu; Guo, An-Yuan Bioinformatics, Vol. 31, Issue 8 https://doi.org/10.1093/bioinformatics/btu817	journal	December 2014
Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane Ozeki, S. Journal of Cell Science, Vol. 118, Issue 12 https://doi.org/10.1242/jcs.02401	journal	June 2005
A Rab-E GTPase Mutant Acts Downstream of the Rab-D Subclass in Biosynthetic Membrane Traffic to the Plasma Membrane in Tobacco Leaf Epidermis Zheng, Huanquan; Camacho, Luísa; Wee, Edmund The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.031112	journal	June 2005
Analysis of the Small GTPase Gene Superfamily of Arabidopsis Vernoud, Vanessa; Horton, Amy C.; Yang, Zhenbiao Plant Physiology, Vol. 131, Issue 3 https://doi.org/10.1104/pp.013052	journal	January 2003
Arabidopsis RABA1 GTPases are involved in transport between the trans -Golgi network and the plasma membrane, and are required for salinity stress tolerance Asaoka, Rin; Uemura, Tomohiro; Ito, Jun The Plant Journal, Vol. 73, Issue 2 https://doi.org/10.1111/tpj.12023	journal	November 2012
PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences Lescot, M. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.325	journal	January 2002
Rab proteins as membrane organizers Zerial, Marino; McBride, Heidi Nature Reviews Molecular Cell Biology, Vol. 2, Issue 2 https://doi.org/10.1038/35052055	journal	February 2001
The Evolutionary Fate and Consequences of Duplicate Genes Lynch, M. Science, Vol. 290, Issue 5494 https://doi.org/10.1126/science.290.5494.1151	journal	November 2000
Membrane targeting mechanism of Rab GTPases elucidated by semisynthetic protein probes Wu, Yao-Wen; Oesterlin, Lena K.; Tan, Kui-Thong Nature Chemical Biology, Vol. 6, Issue 7 https://doi.org/10.1038/nchembio.386	journal	May 2010
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update Tian, Tian; Liu, Yue; Yan, Hengyu Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx382	journal	May 2017
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Tuskan, G. A.; DiFazio, S.; Jansson, S. Science, Vol. 313, Issue 5793, p. 1596-1604 https://doi.org/10.1126/science.1128691	journal	September 2006
Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana Yu, Lijuan; Nie, Jianing; Cao, Chunyan New Phytologist, Vol. 188, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03422.x	journal	August 2010
Membrane fusion Wickner, William; Schekman, Randy Nature Structural & Molecular Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nsmb.1451	journal	July 2008
Constitutive overexpression of a stress-inducible small GTP-binding protein PgRab7 from Pennisetum glaucum enhances abiotic stress tolerance in transgenic tobacco Agarwal, Pradeep K.; Agarwal, Parinita; Jain, Parul Plant Cell Reports, Vol. 27, Issue 1 https://doi.org/10.1007/s00299-007-0446-0	journal	September 2007
Subcellular Localization and Functional Analysis of the Arabidopsis GTPase RabE Speth, Elena Bray; Imboden, Lori; Hauck, Paula Plant Physiology, Vol. 149, Issue 4 https://doi.org/10.1104/pp.108.132092	journal	February 2009
Cytoscape 2.8: new features for data integration and network visualization Smoot, M. E.; Ono, K.; Ruscheinski, J. Bioinformatics, Vol. 27, Issue 3 https://doi.org/10.1093/bioinformatics/btq675	journal	December 2010
Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes Ren, M.; Xu, G.; Zeng, J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.6187	journal	May 1998
Distinct Localization of Two Closely Related Ypt3/Rab11 Proteins on the Trafficking Pathway in Higher Plants Inaba, Takehito; Nagano, Yukio; Nagasaki, Takeshi Journal of Biological Chemistry, Vol. 277, Issue 11 https://doi.org/10.1074/jbc.M111491200	journal	December 2001
The Heat Shock Factor A4A Confers Salt Tolerance and Is Regulated by Oxidative Stress and the Mitogen-Activated Protein Kinases MPK3 and MPK6 Pérez-Salamó, Imma; Papdi, Csaba; Rigó, Gábor Plant Physiology, Vol. 165, Issue 1 https://doi.org/10.1104/pp.114.237891	journal	March 2014
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
WUSCHEL-related Homeobox genes in Populus tomentosa: diversified expression patterns and a functional similarity in adventitious root formation Liu, Bobin; Wang, Lin; Zhang, Jin BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-296	journal	January 2014
The role of the hypervariable C-terminal domain in Rab GTPases membrane targeting Li, F.; Yi, L.; Zhao, L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 7 https://doi.org/10.1073/pnas.1313655111	journal	February 2014
Functions of RAB and SNARE Proteins in Plant Life Saito, Chieko; Ueda, Takashi International Review of Cell and Molecular Biology, Vol. 274, p. 182-233 https://doi.org/10.1016/S1937-6448(08)02004-2	book	January 2009
Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses Zhang, Jin; Li, Jianbo; Liu, Bobin BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-532	journal	January 2013
Characterization of in vivo functions of Nicotiana benthamiana RabE1 Ahn, Chang Sook; Han, Jeong-A; Pai, Hyun-Sook Planta, Vol. 237, Issue 1 https://doi.org/10.1007/s00425-012-1760-5	journal	September 2012
Plant vacuolar trafficking driven by RAB and SNARE proteins Uemura, Tomohiro; Ueda, Takashi Current Opinion in Plant Biology, Vol. 22 https://doi.org/10.1016/j.pbi.2014.10.002	journal	December 2014
Rab2 GTPase Regulates Vesicle Trafficking between the Endoplasmic Reticulum and the Golgi Bodies and Is Important to Pollen Tube Growth Cheung, Alice Y.; Chen, Christine Y. -h.; Glaven, Richard H. The Plant Cell, Vol. 14, Issue 4 https://doi.org/10.1105/tpc.000836	journal	April 2002
TIP47 is a key effector for Rab9 localization Aivazian, Dikran; Serrano, Ramon L.; Pfeffer, Suzanne Journal of Cell Biology, Vol. 173, Issue 6 https://doi.org/10.1083/jcb.200510010	journal	June 2006
A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants Batoko, Henri; Zheng, Huan-Quan; Hawes, Chris The Plant Cell, Vol. 12, Issue 11 https://doi.org/10.1105/tpc.12.11.2201	journal	November 2000
A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6 Ebine, Kazuo; Fujimoto, Masaru; Okatani, Yusuke Nature Cell Biology, Vol. 13, Issue 7 https://doi.org/10.1038/ncb2270	journal	June 2011
Evolution of the rab family of small GTP-binding proteins Pereira-Leal, José B.; Seabra, Miguel C. Journal of Molecular Biology, Vol. 313, Issue 4 https://doi.org/10.1006/jmbi.2001.5072	journal	November 2001
Membrane fusion Jahn, Reinhard; Grubmüller, Helmut Current Opinion in Cell Biology, Vol. 14, Issue 4 https://doi.org/10.1016/s0955-0674(02)00356-3	journal	August 2002
A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants Batoko, Henri; Zheng, Huan-Quan; Hawes, Chris The Plant Cell, Vol. 12, Issue 11 https://doi.org/10.2307/3871115	journal	November 2000
inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains Olm, Matthew R.; Crits-Christoph, Alexander; Bouma-Gregson, Keith Nature Biotechnology, Vol. 39, Issue 6 https://doi.org/10.1038/s41587-020-00797-0	journal	January 2021
Functional characterization of an inducible bidirectional promoter from Fusarium oxysporum f. sp. cubense Dash, Ashutosh; Gurdaswani, Vartika; D’Souza, Jacinta S. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-59159-0	journal	February 2020
Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice Harris, Richard; Dussault, Forest; Flint, Annika Microbiology Resource Announcements, Vol. 10, Issue 1 https://doi.org/10.1128/mra.01111-20	journal	January 2021
Membrane fusion Zimmerberg, Joshua; Chernomordik, Leonid V. Advanced Drug Delivery Reviews, Vol. 38, Issue 3 https://doi.org/10.1016/s0169-409x(99)00029-0	journal	August 1999
Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass Xu, Xiaoheng; Feng, Guangyan; Huang, Linkai Molecular Biology Reports, Vol. 47, Issue 3 https://doi.org/10.1007/s11033-020-05279-9	journal	February 2020
Cell signaling under salt, water and cold stresses Zhu, Jian-Kang Current Opinion in Plant Biology, Vol. 4, Issue 5 https://doi.org/10.1016/s1369-5266(00)00192-8	journal	October 2001
Morphogen gradient scaling by recycling of intracellular Dpp Romanova-Michaelides, Maria; Hadjivasiliou, Zena; Aguilar-Hidalgo, Daniel Nature, Vol. 602, Issue 7896 https://doi.org/10.1038/s41586-021-04346-w	journal	December 2021
Variant phasing and haplotypic expression from long-read sequencing in maize Wang, Bo; Tseng, Elizabeth; Baybayan, Primo Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-0805-8	journal	February 2020
Activation of MAPK Kinase 9 Induces Ethylene and Camalexin Biosynthesis and Enhances Sensitivity to Salt Stress in Arabidopsis Xu, Juan; Li, Yuan; Wang, Ying Journal of Biological Chemistry, Vol. 283, Issue 40 https://doi.org/10.1074/jbc.m801392200	journal	August 2008
Arabidopsis - a powerful model system for plant cell wall research Liepman, Aaron H.; Wightman, Raymond; Geshi, Naomi The Plant Journal, Vol. 61, Issue 6 https://doi.org/10.1111/j.1365-313x.2010.04161.x	journal	March 2010

Cited By (3)

De novo transcriptome analysis of Fraxinus velutina Torr in response to NaCl stress Yan, Liping; Liu, Cuilan; Wang, Yinhua Tree Genetics & Genomes, Vol. 15, Issue 4 https://doi.org/10.1007/s11295-019-1340-y	journal	June 2019
Genome-Wide Identification and Characterization of JAZ Protein Family in Two Petunia Progenitors Tian, Shaoze; Liu, Siyu; Wang, Yu Plants, Vol. 8, Issue 7 https://doi.org/10.3390/plants8070203	journal	July 2019
Intracellular Vesicle Trafficking Genes, RabC-GTP, Are Highly Expressed Under Salinity and Rapid Dehydration but Down-Regulated by Drought in Leaves of Chickpea (Cicer arietinum L.) Khassanova, Gulmira; Kurishbayev, Akhylbek; Jatayev, Satyvaldy Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00040	journal	February 2019

Linked Research (32)

Similar Records

GENETIC MODIFICATION OF GIBBERELLIC ACID SIGNALING TO PROMOTE CARBON SEQUESTRATION IN TREE ROOTS AND STEMS

Technical Report · Tue Mar 05 00:00:00 EST 2013 · OSTI ID:1626849

Busov, Victor

Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa

Journal Article · Wed Jan 08 00:00:00 EST 2020 · Frontiers in Plant Science · OSTI ID:1626849

Su, Tao; Han, Mei; Min, Jie; +4 more

The Populus Superoxide Dismutase Gene Family and Its Responses to Drought Stress in Transgenic Poplar Overexpressing a Pine Cytosolic Glutamine Synthetase (GS1a)

Journal Article · Fri Feb 22 00:00:00 EST 2013 · PLoS ONE · OSTI ID:1626849

Molina-Rueda, Juan Jesús; Tsai, Chung Jui; Kirby, Edward G.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
Plant Sciences
Populus
Rab GTPase
Phylogenetic analysis
Co-expression network
Subcellular localization
Salt tolerance

Additional file 10: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600107 The current record is supplemented by this image	image	January 2018
Additional file 10: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600107.v1 The current record is supplemented by this image	image	January 2018
Additional file 11: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600131 The current record is supplemented by this dataset	dataset	January 2018
Additional file 11: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600131.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 12: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600152 The current record is supplemented by this dataset	dataset	January 2018
Additional file 12: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600152.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 13: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600173 The current record is supplemented by this image	image	January 2018
Additional file 13: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600173.v1 The current record is supplemented by this image	image	January 2018
Additional file 14: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600197 The current record is supplemented by this image	image	January 2018
Additional file 14: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600197.v1 The current record is supplemented by this image	image	January 2018
Additional file 15: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600209 The current record is supplemented by this text	text	January 2018
Additional file 15: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600209.v1 The current record is supplemented by this text	text	January 2018
Additional file 1: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600239 The current record is supplemented by this text	text	January 2018
Additional file 1: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600239.v1 The current record is supplemented by this text	text	January 2018
Additional file 2: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600269 The current record is supplemented by this image	image	January 2018
Additional file 2: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600269.v1 The current record is supplemented by this image	image	January 2018
Additional file 3: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600293 The current record is supplemented by this image	image	January 2018
Additional file 3: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600293.v1 The current record is supplemented by this image	image	January 2018
Additional file 4: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600308 The current record is supplemented by this image	image	January 2018
Additional file 4: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600308.v1 The current record is supplemented by this image	image	January 2018
Additional file 5: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600332 The current record is supplemented by this image	image	January 2018
Additional file 5: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600332.v1 The current record is supplemented by this image	image	January 2018
Additional file 6: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600353 The current record is supplemented by this image	image	January 2018
Additional file 6: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600353.v1 The current record is supplemented by this image	image	January 2018
Additional file 7: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600365 The current record is supplemented by this text	text	January 2018
Additional file 7: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600365.v1 The current record is supplemented by this text	text	January 2018
Additional file 8: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.6600380 The current record is supplemented by this dataset	dataset	January 2018
Additional file 8: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600380.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 9: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600404 The current record is supplemented by this image	image	January 2018
Additional file 9: of Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.6600404.v1 The current record is supplemented by this image	image	January 2018
Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/M9.FIGSHARE.C.4137464 The current record is supplemented by this collection	collection	January 2018
Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance Zhang, Jin; Li, Yu; Liu, Bobin https://doi.org/10.6084/m9.figshare.c.4137464.v1 The current record is supplemented by this collection	collection	January 2018