Characterization of the XTH Gene Family: New Insight to the Roles in Soybean Flooding Tolerance
<p>An unrooted phylogenetic tree for <span class="html-italic">AtXTH</span>, <span class="html-italic">OsXTH</span>, and <span class="html-italic">GmXTH</span> genes. A phylogenetic tree was constructed using the neighbor-joining method implemented in MEGA7. The number beside the branches represents bootstrap values based on 1000 replications. The XTH members are classified into three subfamilies. Genes from groups I/II and III are shown in the black and red/pink lines, respectively. Group III was designated group IIIA (red) and group IIIB (pink).</p> "> Figure 2
<p>Chromosomal location of 61 <span class="html-italic">GmXTH</span> genes along soybean’s 20 chromosomes. Physical map showed the distribution of the <span class="html-italic">Glycine max XTH</span> genes along the 20 chromosomes with colors indicating duplicated gene pairs. The chromosome number is indicated at the bottom.</p> "> Figure 3
<p>Conserved protein motifs in soybean XTHs. (<b>A</b>) Motifs in XTH protein sequences of 61 GmXTH identified with the MEME tool. (<b>B</b>) Alignment of the putative-site amino acid residues in group III XTH proteins from <span class="html-italic">Arabidopsis</span>, rice, and soybean constructed with the CLUSTALW2 program. Amino acid residues that are identical within this motif are indicated by gray shading. “*” means that the residues or nucleotides in that column are identical in all sequences in the alignment. “:” means that conserved substitutions have been observed.</p> "> Figure 4
<p>Heatmap of the expression profiles of the <span class="html-italic">GmXTH</span> gene family in nine organs. Relative organ expression levels of <span class="html-italic">GmXTHs</span> based on RNA-seq data were used to construct the heatmap. The expression values (Reads Per Kilobase Million) were median-cantered and normalized for each gene in different tissues before transforming to color scale. The color bar at the bottom shows the range of expression values from highest expression level (red) to lowest expression level (green), and 0 is the median expression level (Black). SAM (Shoot Apical Meristem).</p> "> Figure 5
<p>Expression patterns of individual <span class="html-italic">XTH</span> genes in response to flooding and ACC treatment studied by qRT-PCR or RNA-seq. (<b>A</b>) Expression pattern of individual <span class="html-italic">XTH</span> genes in response to 24 h flooding treatment in root and hypocotyl organs of two-day-old soybean seedlings. (<b>B</b>,<b>C</b>) Organ-specific expression analysis showed that most <span class="html-italic">XTH</span> genes were unregulated by the ACC in the root tissue, but there was no significant difference in the aerial parts of the three-week-old soybean. Three flooding-related homologous marker genes in soybean were studied as positive controls. Fold change (Log2) of relative gene expression (Actin (Glyma.18G290800)) of soybean was used as the normalization control.</p> "> Figure 6
<p>Calculation of transgene AtXTH31 copy numbers and relative expression levels in four transgenic events. (<b>A</b>) Ratios of copy number between <span class="html-italic">AtXTH31</span> and lectin gene (Glyma.02G009600) were determined by digital PCR in soybean T0 transgenic generation. Soybean transgenic plants contained a single insert copy when the ratio value was equal to 0.5 and two insert copies when the ratio value was equal to 1. (<b>B</b>) The relative expression of <span class="html-italic">AtXTH31</span> in T3 homozygous transgenic soybean roots determined by qRT-PCR. The relative levels of transcripts were normalized to the soybean actin gene (Glyma.18G290800). Bars represent mean values of three biological replicates (standard error). * indicates significantly different at <span class="html-italic">p</span> < 0.05 as tested by Fisher’s least significant difference. Non-transgenic Maverick soybean as a control and MYB2:AtXTH31 transgenic soybean lines ND-30-2, ND-30-9, ND-30-11, and ND-30-12 with overexpression of <span class="html-italic">AtXTH31</span> were studied.</p> "> Figure 7
<p>Soybean <span class="html-italic">AtXTH31</span> transgenic plants show an enhanced germination ratio and elongated root and hypocotyl under flooding conditions. (<b>A</b>) Two-day-old seedlings were flooded with water for 5 days. Bar indicates 1 cm. (<b>B</b>) The germination rate of transgenic and wild-type plants under 7 days of flooding. (<b>C</b>) Length of roots and hypocotyls of flooded Maverick soybean and transgenic seedlings. (<span class="html-italic">n</span> ≥ 30). * indicates differences between the maverick and transgenic soybean (<span class="html-italic">p</span> < 0.05).</p> "> Figure 8
<p>Soybean AtXTH31 transgenic plants show an enhanced flooding tolerance phenotype by promoting adventitious roots, lateral roots, tertiary root tips, and elongated primary roots. (<b>A</b>) Flooding effects on soybean seedlings. The V1 stage seedlings were flooded with water for 7 days. Bar indicates 5 cm. (<b>B</b>) Length of primary root compared between transgenic and control soybean plants under 7 days of flooding conditions. (<b>C</b>–<b>E</b>) The effects of flooding on number of lateral roots, tertiary root tips and adventitious roots per transgenic plant. (<span class="html-italic">n</span> ≥ 20). * indicates differences between the maverick and transgenic soybean (<span class="html-italic">p</span> < 0.05).</p> ">
Abstract
:1. Introduction
2. Results
2.1. Genome-Wide Identification of Soybean XTH Family and Phylogenetic Relationship
2.2. Chromosomal Location and Duplication Process of GmXTHs
2.3. Gene Structure and Conserved Protein Motif Analysis
2.4. GmXTHs Show an Organ-Specific Expression Pattern
2.5. Expression Patterns of GmXTHs Correlated with Flooding Stress
2.6. Stable Transgenic Soybean with Overexpression of AtXTH31
2.7. Transgenic Soybean Exhibits Tolerance to Flooding during the Germination Stage
2.8. Transgenic Soybean Exhibits Tolerance to Flooding during the Vegetative Stage
3. Discussion
3.1. Charaterization of GmXTHs Gene Family
3.2. The Expression Patterns of GmXTHs Were Regulated by Flooding and Ethylene
3.3. The Biological Function of AtXTH31 in Soybean Root Development Under Flooding Stress
3.4. Digital PCR Provides a Simple and Accurate Method for Soybean Transgene Copy Number Analysis
4. Materials & Methods
4.1. Identification, Chromosomal Location, and Structural Organization of GmXTH Family Members in Glycine Max
4.2. Protein Sequence Alignment, Phylogenetic Analysis, and Gene Duplications of GmXTH Genes
4.3. Plant Growth, Hormonal/Flooding Treatments, and Tissue Collection
4.4. Promoter Analysis
4.5. Expression Profiling Using RNA-seq Datasets
4.6. RNA Extraction for Expression Pattern Analysis
4.7. Quantitative RT-PCR Analysis
4.8. Construction of the pZY101-AtXTH31 Vector, Agrobacterium-mediated Soybean (Glycine max) Transformation and Progeny Segregation Analysis
4.9. DNA Extraction and Quantification and PCR Confirmation of Transgenes
4.10. TaqMan Assays and QuantStudio 3D Digital PCR Analysis for Soybean AtXTH31 Transgenic Copy Number Variation
5. Conclusions
Supplementary Materials
Author Contributions
Acknowledgments
Conflicts of Interest
References
- Cantarel, B.L.; Coutinho, P.M.; Rancurel, C.; Bernard, T.; Lombard, V.; Henrissat, B. The Carbohydrate-Active EnZymes database (CAZy): An expert resource for Glycogenomics. Nucleic Acids Res. 2009, D233–D238. [Google Scholar] [CrossRef] [PubMed]
- Fry, S.C.; Smith, R.C.; Renwick, K.F.; Martin, D.J.; Hodge, S.K.; Matthews, K.J. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem. J. 1992, 282, 821–828. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thompson, J.E.; Fry, S.C. Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. Plant J. 2001, 26, 23–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Sandt, V.S.; Suslov, D.; Verbelen, J.P.; Vissenberg, K. Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann. Bot. 2007, 100, 1467–1473. [Google Scholar] [CrossRef] [PubMed]
- Shin, Y.K.; Yum, H.; Kim, E.S.; Cho, H.; Gothandam, K.M.; Hyun, J.; Chung, Y.Y. BcXTH1, a Brassica campestris homologue of Arabidopsis XTH9, is associated with cell expansion. Planta 2006, 224, 32–41. [Google Scholar] [CrossRef] [PubMed]
- Miedes, E.; Herbers, K.; Sonnewald, U.; Lorences, E.P. Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits. J. Agric. Food Chem. 2010, 58, 5708–5713. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Burns, T.H.; Light, G.; Sun, Y.; Fokar, M.; Kasukabe, Y.; Allen, R.D. Xyloglucan endotransglycosylase/hydrolase genes in cotton and their role in fiber elongation. Planta 2010, 232, 1191–1205. [Google Scholar] [CrossRef] [PubMed]
- Shao, M.Y.; Wang, X.D.; Ni, M.; Bibi, N.; Yuan, S.N.; Malik, W.; Zhang, H.P.; Liu, Y.X.; Hua, S.J. Regulation of cotton fiber elongation by xyloglucan endotransglycosylase/hydrolase genes. Genet. Mol. Res. 2011, 10, 3771–3782. [Google Scholar] [CrossRef] [PubMed]
- Nishikubo, N.; Takahashi, J.; Roos, A.A.; Derba-Maceluch, M.; Piens, K.; Brumer, H.; Teeri, T.T.; Stålbrand, H.; Mellerowicz, E.J. Xyloglucan endo-transglycosylase-mediated xyloglucan rearrangements in developing wood of hybrid aspen. Plant Physiol. 2011, 155, 399–413. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.F.; Shi, Y.Z.; Lei, G.J.; Fry, S.C.; Zhang, B.C.; Zhou, Y.H.; Braam, J.; Jiang, T.; Xu, X.Y.; Mao, C.Z.; et al. XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 2012, 24, 4731–4747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.B.; Lu, S.M.; Zhang, J.F.; Liu, S.; Lu, Y.T. A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 2007, 226, 1547–1560. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Spollen, W.G.; Sharp, R.E.; Hetherington, P.R.; Fry, S.C. Root Growth Maintenance at Low Water Potentials (Increased Activity of Xyloglucan Endotransglycosylase and Its Possible Regulation by Abscisic Acid). Plant Physiol. 1994, 106, 607–615. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moore, J.P.; Vicré-Gibouin, M.; Farrant, J.M.; Driouich, A. Adaptations of higher plant cell walls to water loss: Drought vs desiccation. Physiol. Plant. 2008, 134, 237–245. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Jeong, B.R.; Fry, S.C.; Boyer, J.S. Change in XET activities, cell wall extensibility and hypocotyl elongation of soybean seedlings at low water potential. Planta 2005, 220, 593–601. [Google Scholar] [CrossRef] [PubMed]
- Pritchard, J.; Hetherington, P.R.; Fry, S.C.; Tomos, A.D. Xyloglucan endotransglycosylase activity, microfibril orientation and the profiles of cell wall properties along growing regions of maize roots. J. Exp. Bot. 1993, 44, 1281–1289. [Google Scholar] [CrossRef]
- Cho, S.K.; Kim, J.E.; Park, J.A.; Eom, T.J.; Kim, W.T. Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett. 2006, 580, 3136–3144. [Google Scholar] [CrossRef] [PubMed]
- Jan, A.; Yang, G.; Nakamura, H.; Ichikawa, H.; Kitano, H.; Matsuoka, M.; Komatsu, S. Characterization of a xyloglucan endotransglucosylase gene that is up-regulated by gibberellin in rice. Plant Physiol. 2004, 136, 3670–3681. [Google Scholar] [CrossRef] [PubMed]
- Endo, A.; Tatematsu, K.; Hanada, K.; Duermeyer, L.; Okamoto, M.; Yonekura-Sakakibara, K.; Saito, K.; Toyoda, T.; Kawakami, N.; Kamiya, Y.; et al. Tissue-specific transcriptome analysis reveals cell wall metabolism, flavonol biosynthesis and defense responses are activated in the endosperm of germinating Arabidopsis thaliana seeds. Plant Cell Physiol. 2012, 53, 16–27. [Google Scholar] [CrossRef] [PubMed]
- Miura, K.; Lee, J.; Miura, T.; Hasegawa, P.M. SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol. 2010, 51, 103–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saab, I.N.; Sachs, M.M. A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiol. 1996, 112, 385–391. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stacey, G.; Vodkin, L.; Parrott, W.A.; Shoemaker, R.C. National science foundation-sponsored workshop report. Draft plan for soybean genomics. Plant Physiol. 2004, 135, 59–70. [Google Scholar] [CrossRef] [PubMed]
- Manavalan, L.P.; Guttikonda, S.K.; Tran, L.S.; Nguyen, H.T. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 2009, 50, 1260–1276. [Google Scholar] [CrossRef] [PubMed]
- Valliyodan, B.; Ye, H.; Song, L.; Murphy, M.; Shannon, J.G.; Nguyen, H.T. Genetic diversity and genomic strategies for improving drought and waterlogging tolerance in soybeans. J. Exp. Bot. 2017, 68, 1835–1849. [Google Scholar] [CrossRef] [PubMed]
- Ye, H.; Song, L.; Chen, H.; Valliyodan, B.; Ali, L.; Vuong, T.; Wu, C.; Orlowski, J.; Buckley, B.; Chen, P.; et al. A Major Natural Genetic Variation Associated with Root System Architecture and Plasticity Improves Waterlogging Tolerance and Yield in Soybean. Plant Cell Environ. 2018, 41, 2169–2182. [Google Scholar] [CrossRef] [PubMed]
- Nanjo, Y.; Maruyama, K.; Yasue, H.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Komatsu, S. Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol. Biol. 2011, 77, 129–144. [Google Scholar] [CrossRef] [PubMed]
- Zurek, D.M.; Clouse, S.D. Molecular cloning and characterization of a brassinosteroid-regulated gene from elongating soybean (Glycine max L.) epicotyls. Plant Physiol. 1994, 104, 161–170. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, R.; Nishitani, K. A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol. 2001, 42, 1025–1033. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, R.; Rose, J.K.; Nishitani, K. A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol. 2004, 134, 1088–1099. [Google Scholar] [CrossRef] [PubMed]
- Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.; Mitros, T.; Nelson, W.; Hyten, D.L.; Song, Q.; Thelen, J.J.; Cheng, J.; et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178–183. [Google Scholar] [CrossRef] [PubMed]
- Planas, A.; Juncosa, M.; Lloberas, J.; Querol, E. Essential catalytic role of Glu134 in endo-β-1,3-1,4-d-glucan 4-glucanohydrolase from B. licheniformis as determined by site-directed mutagenesis. FEBS Lett. 1992, 308, 141–145. [Google Scholar] [CrossRef]
- Juncosa, M.; Pons, J.; Dot, T.; Querol, E.; Planas, A. Identification of active site carboxylic residues in Bacillus licheniformis 1,3-1,4-beta-d-glucan 4-glucanohydrolase by site-directed mutagenesis. J. Biol. Chem. 1994, 269, 14530–14535. [Google Scholar] [PubMed]
- Libault, M.; Farmer, A.; Joshi, T.; Takahashi, K.; Langley, R.J.; Franklin, L.D.; He, J.; Xu, D.; May, G.; Stacey, G. An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 2010, 63, 86–99. [Google Scholar] [CrossRef] [PubMed]
- Tamang, B.G.; Magliozzi, J.O.; Maroof, M.A.S.; Fukao, T. Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings. Plant, Cell Environ. 2014, 37, 2350–2365. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Yao, Q.; Patil, G.B.; Agarwal, G.; Deshmukh, R.K.; Lin, L.; Wang, B.; Wang, Y.; Prince, S.J.; Song, L.; et al. Identification and Comparative Analysis of Differential Gene Expression in Soybean Leaf Tissue under Drought and Flooding Stress Revealed by RNA-Seq. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Komatsu, S.; Deschamps, T.; Hiraga, S.; Kato, M.; Chiba, M.; Hashiguchi, A.; Tougou, M.; Shimamura, S.; Yasue, H. Characterization of a novel flooding stress-responsive alcohol dehydrogenase expressed in soybean roots. Plant Mol. Biol. 2011, 77, 309–322. [Google Scholar] [CrossRef] [PubMed]
- Kürsteiner, O.; Dupuis, I.; Kuhlemeier, C. The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol. 2003, 132, 968–978. [Google Scholar] [CrossRef] [PubMed]
- Hattori, Y.; Nagai, K.; Furukawa, S.; Song, X.J.; Kawano, R.; Sakakibara, H.; Wu, J.; Matsumoto, T.; Yoshimura, A.; Kitano, H.; et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 2009, 460, 1026–1030. [Google Scholar] [CrossRef] [PubMed]
- Strohmeier, M.; Hrmova, M.; Fischer, M.; Harvey, A.J.; Fincher, G.B.; Pleiss, J. Molecular modeling of family GH16 glycoside hydrolases: Potential roles for xyloglucan transglucosylases/hydrolases in cell wall modification in the poaceae. Protein Sci. 2004, 13, 3200–3213. [Google Scholar] [CrossRef] [PubMed]
- Geisler-Lee, J.; Geisler, M.; Coutinho, P.M.; Segerman, B.; Nishikubo, N.; Takahashi, J.; Aspeborg, H.; Djerbi, S.; Master, E.; Andersson-Gunnerås, S.; et al. Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol. 2006, 140, 946–962. [Google Scholar] [CrossRef] [PubMed]
- Saladié, M.; Rose, J.K.; Cosgrove, D.J.; Catalá, C. Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J. 2006, 47, 282–295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yokoyama, R.; Uwagaki, Y.; Sasaki, H.; Harada, T.; Hiwatashi, Y.; Hasebe, M.; Nishitani, K. Biological implications of the occurrence of 32 members of the XTH (xyloglucan endotransglucosylase/hydrolase) family of proteins in the bryophyte Physcomitrella patens. Plant J. 2010, 64, 645–656. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Linkemer, G.; Board, J.E.; Musgrave, M.E. Waterlogging effects on growth and yield components in late-planted soybean. Crop Sci. 1998, 38, 1576–1584. [Google Scholar] [CrossRef] [PubMed]
- Wuebker, E.F.; Mullen, R.E.; Koehler, K. Flooding and temperature effects on soybean germination. Crop Sci. 2001, 41, 1857–1861. [Google Scholar] [CrossRef]
- Vartapetian, B.B.; Jackson, M.B. Plant adaptations to anaerobic stress. Ann. Bot. 1997, 79, 3–20. [Google Scholar] [CrossRef]
- Komatsu, S.; Yamamoto, R.; Nanjo, Y.; Mikami, Y.; Yunokawa, H.; Sakata, K. A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. J. Proteome Res. 2009, 8, 4766–4778. [Google Scholar] [CrossRef] [PubMed]
- Jackson, M.B.; Colmer, T.D. Response and adaptation by plants to flooding stress. Ann. Bot. 2005, 96, 501–505. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.H.; Hwang, S.J.; Waqas, M.; Khan, A.L.; Lee, J.H.; Lee, J.D.; Nguyen, H.T.; Lee, I.J. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front. Plant Sci. 2015, 6, 714. [Google Scholar] [CrossRef] [PubMed]
- Ookawara, R.; Satoh, S.; Yoshioka, T.; Ishizawa, K. Expression ofα-expansin and xyloglucan endotransglucosylase/hydrolase genes associated with shoot elongation enhanced by anoxia, ethylene and carbon dioxide in arrowhead (Sagittaria pygmaea Miq.) tubers. Ann. Bot. 2005, 96, 693–702. [Google Scholar] [CrossRef] [PubMed]
- Markakis, M.N.; De Cnodder, T.; Lewandowski, M.; Simon, D.; Boron, A.; Balcerowicz, D.; Doubbo, T.; Taconnat, L.; Renou, J.P.; Höfte, H.; et al. Identification of genes involved in the ACC-mediated control of root cell elongation in Arabidopsis thaliana. BMC Plant Biol. 2012, 12, 208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cho, H.T.; Cosgrove, D.J. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 2002, 14, 3237–3253. [Google Scholar] [CrossRef] [PubMed]
- Hashiguchi, A.; Sakata, K.; Komatsu, S. Proteome analysis of early-stage soybean seedlings under flooding stress. J. Proteome Res. 2009, 8, 2058–2069. [Google Scholar] [CrossRef] [PubMed]
- Baumann, M.J.; Eklöf, J.M.; Michel, G.; Kallas, A.M.; Teeri, T.T.; Czjzek, M.; Brumer, H. 3rd. Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: Biological implications for cell wall metabolism Fry. Plant Cell 2007, 9, 1947–1963. [Google Scholar] [CrossRef] [PubMed]
- Sakazono, S.; Nagata, T.; Matsuo, R.; Kajihara, S.; Watanabe, M.; Ishimoto, M.; Shimamura, S.; Harada, K.; Takahashi, R.; Mochizuki, T. Variation in root development response to flooding among 92 soybean lines during early growth stages. Plant Prod. Sci. 2014, 17, 228–236. [Google Scholar] [CrossRef]
- Jitsuyama, Y. Morphological root responses of soybean to rhizosphere hypoxia reflect waterlogging tolerance. Can. J. Plant Sci. 2015, 95, 999–1005. [Google Scholar] [CrossRef] [Green Version]
- Valliyodan, B.; Van Toai, T.T.; Alves, J.D.; de Fátima, P.; Goulart, P.; Lee, J.D.; Fritschi, F.B.; Rahman, M.A.; Islam, R.; Shannon, J.G.; et al. Expression of root-related transcription factors associated with flooding tolerance of soybean (Glycine max). Int. J. Mol. Sci. 2014, 15, 17622–17643. [Google Scholar] [CrossRef] [PubMed]
- Corbisier, P.; Bhat, S.; Partis, L.; Xie, V.R.; Emslie, K.R. Absolute quantification of genetically modified MON810 maize (Zea mays L.) by digital polymerase chain reaction. Anal. Bioanal. Chem. 2010, 396, 2143–2150. [Google Scholar] [CrossRef] [PubMed]
- Wan, J.R.; Song, L.; Wu, Y.L.; Brzoska, P.; Keys, D.; Chen, C.F.; Valliyodan, B.; Shannon, J.G.; Nguyen, T.H. Application of Digital PCR in the Analysis of Transgenic Soybean Plants. Adv. Biosci. Biotechnol. 2016, 7, 403–417. [Google Scholar] [CrossRef]
- Collier, R.; Dasgupta, K.; Xing, Y.P.; Hernandez, B.T.; Shao, M.; Rohozinski, D.; Kovak, E.; Lin, J.; de Oliveira, M.L.P.; Stover, E.; et al. Accurate measurement of transgene copy number in crop plants using droplet digital PCR. Plant J. 2017, 90, 1014–1025. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, B.; Jin, J.; Guo, A.Y.; Zhang, H.; Luo, J.; Gao, G. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics 2015, 3, 1296–1297. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuckerkandl, E.; Pauling, L. Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins; Bryson, V., Vogel, H.J., Eds.; Academic Press: New York, NY, USA, 1965; pp. 97–166. [Google Scholar]
- Lynch, M.; Conery, J.S. The evolutionary fate and consequences of duplicate genes. Science 2000, 290, 1151–1155. [Google Scholar] [CrossRef] [PubMed]
- Koressaar, T.; Remm, M. Enhancements and modifications of primer design program Primer3. Bioinformatics 2007, 23, 1289–1291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Untergasser, A.; Cutcutache, I.; Koressaar, T.; Ye, J.; Faircloth, B.C.; Remm, M.; Rozen, S.G. Primer3-new capabilities and interfaces. Nucleic Acids Res. 2012, 40, E115. [Google Scholar] [CrossRef] [PubMed]
- Zeng, P.; Vadnais, D.; Zhang, Z.; Polacco, J. Refined glufosinate selection in Agrobacterium-mediated transformation of soybean [Glycine max (L.) Merr.]. Plant Cell Rep. 2004, 22, 478–482. [Google Scholar] [CrossRef] [PubMed]
- Vuong, T.D.; Sleper, D.A.; Shannon, J.G.; Nguyen, H.T. Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C. Theor. Appl. Genet. 2010, 121, 1253–1266. [Google Scholar] [CrossRef] [PubMed]
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Song, L.; Valliyodan, B.; Prince, S.; Wan, J.; Nguyen, H.T. Characterization of the XTH Gene Family: New Insight to the Roles in Soybean Flooding Tolerance. Int. J. Mol. Sci. 2018, 19, 2705. https://doi.org/10.3390/ijms19092705
Song L, Valliyodan B, Prince S, Wan J, Nguyen HT. Characterization of the XTH Gene Family: New Insight to the Roles in Soybean Flooding Tolerance. International Journal of Molecular Sciences. 2018; 19(9):2705. https://doi.org/10.3390/ijms19092705
Chicago/Turabian StyleSong, Li, Babu Valliyodan, Silvas Prince, Jinrong Wan, and Henry T. Nguyen. 2018. "Characterization of the XTH Gene Family: New Insight to the Roles in Soybean Flooding Tolerance" International Journal of Molecular Sciences 19, no. 9: 2705. https://doi.org/10.3390/ijms19092705