Allele-Specific Hormone Dynamics in Highly Transgressive F2 Biomass Segregants in Sugarcane (Saccharum spp.)
<p>Partial least squares-discriminant analysis (PLS-DA), Hierarchical clustering, and volcano plot of DEGs: (<b>A</b>) PLS-DA score plot of FPKM data of DEGs generated by using preprocessed original data shows the clustering of extreme biomass segregants. Component 1 (26%) clearly distinguishes the two biomass groups. (<b>B</b>) (<b>a</b>) Hierarchical clustering heatmap of the DEGs based on FPKM expression values, (<b>b</b>) Six clusters indicating the up and down regulated genes identified in heatmap. (<b>C</b>) Volcano plot overall shows the range of log2FC of DEGs, i.e., 24 to −26 from right to left.</p> "> Figure 2
<p>KEGG and GO analysis of DEGs: (<b>A</b>) Bar plot for the KEGG categories and enriched DEGs in KEGG analysis. The abscissa depicts enriched pathways while gene number is plotted on an ordinate axis. (<b>B</b>) GO shows the enrichment of potential DEGs in different categories, i.e., biological processes, cellular components, and molecular function.</p> "> Figure 3
<p>Heatmap of log2FC values in HB segregants. Red and black values in legend show down and upregulated genes. (<b>A</b>) shows ubiquitin-mediated signaling of auxin and jasmonic acid signaling pathways. (<b>B</b>) depicts the expression patterns of hormone-responsive growth-related genes in cell wall and terminal developmental phases, i.e., inflorescence and senescence. <span class="html-italic">S-40</span>: Senescence regulator, <span class="html-italic">ATHB</span>: ARABIDOPSIS THALIANA HOMEOBOX 7, <span class="html-italic">KNAT1</span>: BREVIPEDICELLUS, <span class="html-italic">PHOX2/ARIX</span>: Transcription factor PHOX2/ARIX, <span class="html-italic">ELF3</span>: EARLY FLOWERING 3 (<span class="html-italic">ELF3</span>), <span class="html-italic">FPF1</span>: FLOWERING PROMOTING FACTOR 1, <span class="html-italic">AGAMOUS-LIKE 12</span>: AGAMOUS-LIKE 12, <span class="html-italic">XXT</span>: galactosyl transferase GMA12/MNN10 family, <span class="html-italic">EXPANSIN</span>: EXPANSIN, <span class="html-italic">CESA</span>: cellulose synthase subfamily, <span class="html-italic">GAE</span>: GDP-mannose 4,6 dehydratase, <span class="html-italic">CSLA02</span>: belongs to the glycosyltransferase 2 family, <span class="html-italic">XTH</span>: Xyloglucan endohydrolysis (<span class="html-italic">XEH</span>) and or endotransglycosylation (<span class="html-italic">XET</span>), and <span class="html-italic">UGT</span>: UDP-glycosyltransferase family.</p> "> Figure 4
<p>Weighted gene co-expression network analysis (WGCNA) of DEGs between HB and LB segregants. (<b>A</b>) eigengene modules, module–trait relationship, and module–module relationship. Module–trait heatmap shows Pearson’s correlation of all the modules with samples, whereas in the module–module relationship, progressive saturation in blue and red color points to high co-expression interconnectedness. Additionally, it shows dendrogram of module clustering, with green and red horizontal lines representing threshold (0.25, 0.3). (<b>B</b>) Cytoscape network shows co-expression network of blue module, which depicts highly upregulated genes in HB segregants (<b>C</b>) Cystoscape network of overrepresented DEGs in module “greenyellow”. Size and color of nodes are proportional to weights, whereas edge colors correspond to module names.</p> "> Figure 5
<p>Heatmap generated using log2FC. Expression dynamics of TFs and PKs involved in high biomass samples. Green and blue scales represent up and downregulated TFs in HB samples, whereas grey color indicates blanks.</p> "> Figure 6
<p>(<b>A</b>) Concentrations of the endogenous hormones, i.e., ABA, JA, and IAA, in the leaves of high and low biomass F2 segregants. Bar charts present the means with error bars showing standard errors, different letters are based on one-way ANOVA and LSD tests at α = 0.05. (<b>B</b>) Linear regression model of hormone content and qPCR values of the genes identified in RNA-Seq. analysis in the respective signaling pathway.</p> "> Figure 7
<p>Confirmation of FPKM by qPCR expression. Green bars represent the relative expression in qPCR, and orange lines represent FPKM values in transcriptome for corresponding genes. Values on the <span class="html-italic">y</span>-axis indicate relative expression levels of qPCR (<b>left</b>) and RNA-Seq (<b>right</b>). Error bars show standard error of the means at (<span class="html-italic">p</span> < 0.05), and “r” is indicative of correlation between qPCR and FPKM expression values.</p> ">
Abstract
:1. Introduction
2. Results
2.1. Sequence Read Alignment and Differential Expression Analysis
2.2. Exploration of Biological Processes Involved in Growth and Biomass by GO
2.3. Hormone Dynamics in Extreme Segregants
2.4. Auxin-Related Genes
2.5. Jasmonic Acid (JA) Signaling Pathway Genes
2.6. Abscisic Acid (ABA)-Related Genes
2.7. Hormone-Responsive Genes Accounting for Growth
2.8. Flowering and Senescence Genes Downregulated in High-Biomass Group
2.9. Identification of WGCNA Modules Associated with Hormone and Cell Wall Expansion Genes
2.10. Expression Profiles of Transcription Factors and Protein Kinases (Kinome)
2.11. Hormone Quantification
2.12. RNA-Seq Data Validation by qRT-PCR
3. Discussion
4. Materials and Methods
4.1. Background of RNA-Seq Reads
- a.
- Sequence read alignment and analysis of differentially expressed genes
4.2. Functional Annotation and GO Enrichment Analysis
4.3. KEGG Analysis, Transcription Factor and Kinome
4.4. Weighted Gene Co-Expression Analysis (WGCNA) Analysis
4.5. Hormones Quantification
4.6. Quantitative RT-PCR-Based Quantification for Gene Expression
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Bessou, C.; Ferchaud, F.; Gabrielle, B.; Mary, B. Biofuels, greenhouse gases and climate change. In Sustainable Agriculture; Springer: Dordrecht, The Netherlands, 2009; pp. 365–468. [Google Scholar] [CrossRef]
- IEA. Key World Energy Statistics 2021; International Energy Agency: Paris, France, 2021; Available online: https://www.iea.org (accessed on 17 April 2022).
- Work, V.H.; D’Adamo, S.; Radakovits, R.; Jinkerson, R.E.; Posewitz, M.C. Improving photosynthesis and metabolic networks for the competitive production of phototroph-derived biofuels. Curr. Opin. Biotechnol. 2012, 23, 290–297. [Google Scholar] [CrossRef]
- Hofsetz, K.; Silva, M.A. Brazilian sugarcane bagasse: Energy; non-energy consumption. Biomass Bioenergy 2012, 46, 564–573. [Google Scholar] [CrossRef]
- Zhang, J.; Zhang, Q.; Li, L.; Tang, H.; Zhang, Q.; Chen, Y.; Arrow, J.; Zhang, X.; Wang, A.; Miao, C.; et al. Recent polyploidization events in three Saccharum founding species. Plant Biotechnol. J. 2019, 17, 264–274. [Google Scholar] [CrossRef] [PubMed]
- Meena, R.K.; Reddy, K.S.; Gautam, R.; Maddela, S.; Reddy, A.R.; Gudipalli, P. Improved photosynthetic characteristics correlated with enhanced biomass in a heterotic F1 hybrid of maize (Zea mays L.). Photosynth. Res. 2021, 147, 253–267. [Google Scholar] [CrossRef] [PubMed]
- Qi, Y.; Gao, X.; Zeng, Q.; Zheng, Z.; Wu, C.; Yang, R.; Feng, X.; Wu, Z.; Fan, L.; Huang, Z.; et al. Sugarcane Breeding, Germplasm Development and Related Molecular Research in China. Sugar Tech 2022, 24, 73–85. [Google Scholar] [CrossRef]
- Sreenivasa, V.; Mahadevaiah, C.; Mahadeva Swamy, H.K.; Raja, A.K.; Meena, M.R.; Appunu, C.; Kumar, R.; Mohanraj, K.; Govindaraj, P.; Hemaprabha, G. Deciphering biomass contributing traits of interspecific and intergeneric hybrids derived from early generations hybrids of Saccharum and Erianthus spp. as potential sources of biomass and bioenergy. Ind. Crops Prod. 2024, 211, 118267. [Google Scholar] [CrossRef]
- Ain, N.U.; Haider, F.U.; Fatima, M.; Habiba; Zhou, Y.; Ming, R. Genetic Determinants of Biomass in C4 Crops: Molecular and Agronomic Approaches to Increase Biomass for Biofuels. Front. Plant Sci. 2022, 13, 839588. [Google Scholar] [CrossRef]
- Kandel, R.; Yang, X.; Song, J.; Wang, J. Potentials; challenges, and genetic and genomic resources for sugarcane biomass improvement. Front. Plant Sci. 2018, 9, 151. [Google Scholar] [CrossRef]
- Depuydt, S.; Hardtke, C.S. Hormone Signalling Crosstalk in Plant Growth Regulation. Curr. Biol. 2011, 21, R365–R373. [Google Scholar] [CrossRef]
- Jez, J.M. Connecting primary and specialized metabolism: Amino acid conjugation of phytohormones by GRETCHEN HAGEN 3 (GH3) acyl acid amido synthetases. Curr. Opin. Plant Biol. 2022, 66, 102194. [Google Scholar] [CrossRef]
- Zhu, F.; Wai, C.M.; Zhang, J.; Jones, T.C.; Nagai, C.; Ming, R. Differential expression of hormone related genes between extreme segregants of a Saccharum interspecific F2 population. Euphytica 2018, 214, 55. [Google Scholar] [CrossRef]
- Fukaki, H.; Nakao, Y.; Okushima, Y.; Theologis, A.; Tasaka, M. Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J. 2005, 44, 382–395. [Google Scholar] [CrossRef]
- Rouse, D.; Mackay, P.; Stirnberg, P.; Estelle, M.; Leyser, O. Changes in auxin response from mutations in an AUX/IAA gene. Science 1998, 279, 1371–1373. [Google Scholar] [CrossRef] [PubMed]
- Tatematsu, K.; Kumagai, S.; Muto, H.; Sato, A.; Watahiki, M.K.; Harper, R.M.; Liscum, E.; Yamamoto, K.T. Massugu2 Encodes Aux/IAA19, an Auxin-Regulated Protein That Functions Together with the Transcriptional Activator NPH4/ARF7 to Regulate Differential Growth Responses of Hypocotyl and Formation of Lateral Roots in Arabidopsis thaliana. Plant Cell 2004, 16, 379–393. [Google Scholar] [CrossRef]
- Rogg, L.E.; Lasswell, J.; Bartel, B. A Gain-of-Function Mutation in IAA28 Suppresses Lateral Root Development. 2001. Available online: https://www.plantcell.org (accessed on 22 December 2020).
- Mandaokar, A.; Thines, B.; Shin, B.; Lange, B.M.; Choi, G.; Koo, Y.J.; Yoo, Y.J.; Choi, Y.D.; Choi, G.; Browse, J. Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 2006, 46, 984–1008. [Google Scholar] [CrossRef] [PubMed]
- Sheard, L.; Tan, X.; Mao, H.; Withers, J.; Ben-Nissan, G.; Hinds, T.R.; Kobayashi, Y.; Hsu, F.-F.; Sharon, M.; Browse, J.; et al. Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor. Nature 2010, 468, 400–405. [Google Scholar] [CrossRef] [PubMed]
- Weiner, J.J.; Peterson, F.C.; Volkman, B.F.; Cutler, S.R. Structural and functional insights into core ABA signaling. Curr. Opin. Plant Biol. 2010, 13, 495–502. [Google Scholar] [CrossRef]
- Ma, Y.; Szostkiewicz, I.; Korte, A.; Moes, D.; Yang, Y.; Christmann, A.; Grill, E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 2009, 324, 1064–1068. [Google Scholar] [CrossRef] [PubMed]
- Wai, C.M.; Zhang, J.; Jones, T.C.; Nagai, C.; Ming, R. Cell wall metabolism and hexose allocation contribute to biomass accumulation in high yielding extreme segregants of a Saccharum interspecific F2 population. BMC Genom. 2017, 18, 773. [Google Scholar] [CrossRef]
- Sforça, D.A.; Vautrin, S.; Cardoso-Silva, C.B.; Mancini, M.C.; Romero-da Cruz, M.V.; da Silva Pereira, G.; Conte, M.; Bellec, A.; Dahmer, N.; Fourment, J.; et al. Gene Duplication in the Sugarcane Genome: A Case Study of Allele Interactions and Evolutionary Patterns in Two Genic Regions. Front. Plant Sci. 2019, 10, 553. [Google Scholar] [CrossRef]
- Ganko, E.W.; Meyers, B.C.; Vision, T.J. Divergence in Expression between Duplicated Genes in Arabidopsis. Mol. Biol. Evol. 2007, 24, 2298–2309. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef]
- Wang, S.; Bai, Y.; Shen, C.; Wu, Y.; Zhang, S.; Jiang, D.; Guilfoyle, T.J.; Chen, M.; Qi, Y. Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct. Integr. Genom. 2010, 10, 533–546. [Google Scholar] [CrossRef]
- Singh, K.B.; Foley, R.C.; Oñate-Sánchez, L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002, 5, 430–436. [Google Scholar] [CrossRef]
- Qiao, Z.; Li, C.L.; Zhang, W. WRKY1 regulates stomatal movement in drought-stressed Arabidopsis thaliana. Plant Mol. Biol. 2016, 91, 53–65. [Google Scholar] [CrossRef]
- Schlereth, A.; Möller, B.; Liu, W.; Kientz, M.; Flipse, J.; Rademacher, E.H.; Schmid, M.; Jürgens, G.; Weijers, D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464, 913–916. [Google Scholar] [CrossRef] [PubMed]
- Aono, A.H.; Pimenta, R.J.G.; Garcia, A.L.B.; Correr, F.H.; Hosaka, G.K.; Carrasco, M.M.; Cardoso-Silva, C.B.; Mancini, M.C.; Sforça, D.A.; Santos, L.B.D.; et al. The Wild Sugarcane and Sorghum Kinomes: Insights into Expansion, Diversification, and Expression Patterns. Front. Plant Sci. 2021, 12, 668623. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Zhang, X.; Tang, H.; Zhang, Q.; Hua, X.; Ma, X.; Zhu, F.; Jones, T.; Zhu, X.; Bowers, J.; et al. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat. Genet. 2018, 50, 1565–1573. [Google Scholar] [CrossRef]
- Woodward, A.W.; Bartel, B. Auxin: Regulation, Action, and Interaction. Ann. Bot. 2005, 95, 707–735. [Google Scholar] [CrossRef]
- Chae, K.; Isaacs, C.G.; Reeves, P.H.; Maloney, G.S.; Muday, G.K.; Nagpal, P.; Reed, J.W. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J. 2012, 71, 684–697. [Google Scholar] [CrossRef]
- Spartz, A.K.; Lee, S.H.; Wenger, J.P.; Gonzalez, N.; Itoh, H.; Inzé, D.; Peer, W.A.; Murphy, A.S.; Overvoorde, P.J.; Gray, W.M. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J. 2012, 70, 978–990. [Google Scholar] [CrossRef] [PubMed]
- van Mourik, H.; van Dijk, A.D.J.; Stortenbeker, N.; Angenent, G.C.; Bemer, M. Divergent regulation of Arabidopsis SAUR genes: A focus on the SAUR10-clade. BMC Plant Biol. 2017, 17, 245. [Google Scholar] [CrossRef] [PubMed]
- Spartz, A.K.; Ren, H.; Park, M.Y.; Grandt, K.N.; Lee, S.H.; Murphy, A.S.; Sussman, M.R.; Overvoorde, P.J.; Gray, W.M. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 2014, 26, 2129–2142. [Google Scholar] [CrossRef] [PubMed]
- Feng, S.; Yue, R.; Tao, S.; Yang, Y.; Zhang, L.; Xu, M.; Wang, H.; Shen, C. Genome-wide identification, expression analysis of auxin-responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses. J. Integr. Plant Biol. 2015, 57, 783–795. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y. Auxin biosynthesis: A simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol. Plant. 2012, 5, 334–338. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Zhang, J.; Tang, W.; Huang, Y.; Niu, X.; Zhao, Y.; Han, Y.; Liu, Y. Down-regulation of a LBD-like gene, OsIG1, leads to occurrence of unusual double ovules and developmental abnormalities of various floral organs and megagametophyte in rice. J. Exp. Bot. 2015, 66, 99–112. [Google Scholar] [CrossRef]
- Hickman, R.; Van Verk, M.C.; Van Dijken, A.J.H.; Mendes, M.P.; Vroegop-Vos, I.A.; Caarls, L.; Steenbergen, M.; Van der Nagel, I.; Wesselink, G.J.; Jironkin, A.; et al. Architecture and dynamics of the jasmonic acid gene regulatory network. Plant Cell 2017, 29, 2086–2105. [Google Scholar] [CrossRef]
- Carvalhais, L.C.; Schenk, P.M.; Dennis, P.G. Jasmonic acid signalling and the plant holobiont. Curr. Opin. Microbiol. 2017, 37, 42–47. [Google Scholar] [CrossRef]
- Sivanandhan, G.; Arun, M.; Mayavan, S.; Rajesh, M.; Mariashibu, T.S.; Manickavasagam, M.; Selvaraj, N.; Ganapathi, A. Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L.) Dunal. Ind. Crops Prod. 2012, 37, 124–129. [Google Scholar] [CrossRef]
- Coste, A.; Vlase, L.; Halmagyi, A.; Deliu, C.; Coldea, G. Effects of plant growth regulators and elicitors on production of secondary metabolites in shoot cultures of Hypericum hirsutum and Hypericum maculatum. Plant Cell. Tissue Organ Cult. 2011, 106, 279–288. [Google Scholar] [CrossRef]
- Kim, O.T.; Kim, M.Y.; Hong, M.H.; Ahn, J.C.; Hwang, B. Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) urban by elicitors. Plant Cell Rep. 2004, 23, 339–344. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Turner, J.G. Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis. PLoS ONE 2008, 3, e3699. [Google Scholar] [CrossRef] [PubMed]
- Gutierrez, L.; Mongelard, G.; Floková, K.; Pǎcurar, D.I.; Novák, O.; Staswick, P.; Kowalczyk, M.; Pǎcurar, M.; Demailly, H.; Geiss, G.; et al. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 2012, 24, 2515–2527. [Google Scholar] [CrossRef] [PubMed]
- Cosgrove, D.J. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 2005, 6, 850–861. [Google Scholar] [CrossRef] [PubMed]
- Wolf, S.; Hématy, K.; Höfte, H. Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol. 2012, 63, 381–407. [Google Scholar] [CrossRef] [PubMed]
- Vissenberg, K.; Oyama, M.; Osato, Y.; Yokoyama, R.; Verbelen, J.-P.; Nishitani, K. Differential Expression of AtXTH17, AtXTH18, AtXTH19 and AtXTH20 Genes in Arabidopsis Roots. Physiological Roles in Specification in Cell Wall Construction. Plant Cell Physiol. 2005, 46, 192–200. [Google Scholar] [CrossRef] [PubMed]
- Zhai, D.; Zhang, L.-Y.; Li, L.-Z.; Xu, Z.-G.; Liu, X.-L.; Shang, G.-D.; Zhao, B.; Gao, J.; Wang, F.-X.; Wang, J.-W. Reciprocal conversion between annual and polycarpic perennial flowering behavior in the Brassicaceae. Cell 2024, 187, 3319–3337. [Google Scholar] [CrossRef] [PubMed]
- Venail, J.; da Silva Santos, P.H.; Manechini, J.R.; Alves, L.C.; Scarpari, M.; Falcão, T.; Romanel, E.; Brito, M.; Vicentini, R.; Pinto, L.; et al. Analysis of the PEBP gene family and identification of a novel FLOWERING LOCUS T orthologue in sugarcane. J. Exp. Bot. 2022, 73, 2035–2049. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.; Xie, Q.; Chua, N.H. The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 2003, 15, 1951–1961. [Google Scholar] [CrossRef]
- Habiba; Xu, J.; Gad, A.G.; Luo, Y.; Fan, C.; Uddin, J.B.G.; Ain, N.U.; Huang, C.; Zhang, Y.; Miao, Y.; et al. Five OsS40 Family Members Are Identified as Senescence-Related Genes in Rice by Reverse Genetics Approach. Front. Plant Sci. 2021, 12, 1865. [Google Scholar] [CrossRef]
- D’Esposito, D.; Cappetta, E.; Andolfo, G.; Ferriello, F.; Borgonuovo, C.; Caruso, G.; De Natale, A.; Frusciante, L.; Ercolano, M.R. Deciphering the biological processes underlying tomato biomass production and composition. Plant Physiol. Biochem. 2019, 143, 50–60. [Google Scholar] [CrossRef] [PubMed]
- Ulmasov, T.; Hagen, G.; Guilfoyle, T.J. Activation and repression of transcription by auxin-response factors. Proc. Natl. Acad. Sci. USA 1999, 96, 5844–5849. [Google Scholar] [CrossRef] [PubMed]
- De Smet, I.; Voß, U.; Jürgens, G.; Beeckman, T. Receptor-like kinases shape the plant. Nat. Cell Biol. 2009, 11, 1166–1173. [Google Scholar] [CrossRef]
- Sheen, J. Ca2+-dependent protein kinases and stress signal transduction in plants. Science 1996, 274, 1900–1902. [Google Scholar] [CrossRef] [PubMed]
- Hardin, S.C.; Winter, H.; Huber, S.C. Phosphorylation of the amino terminus of maize sucrose synthase in relation to membrane association and enzyme activity. Plant Physiol. 2004, 134, 1427–1438. [Google Scholar] [CrossRef]
- Hrabak, E.M.; Chan, C.W.M.; Gribskov, M.; Harper, J.F.; Choi, J.H.; Halford, N.; Kudla, J.; Luan, S.; Nimmo, H.G.; Sussman, M.R.; et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 2003, 132, 666–680. [Google Scholar] [CrossRef]
- Munns, R.; Cramer, G.R. Is coordination of leaf and root growth mediated by abscisic acid? Opinion. Plant Soil 1996, 185, 33–49. [Google Scholar] [CrossRef]
- Cheng, W.-H.; Endo, A.; Zhou, L.; Penney, J.; Chen, H.-C.; Arroyo, A.; Leon, P.; Nambara, E.; Asami, T.; Seo, M.; et al. A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions. Plant Cell 2002, 14, 2723–2743. [Google Scholar] [CrossRef] [PubMed]
- Boudsocq, M.; Laurière, C. Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiol. 2005, 138, 1185–1194. [Google Scholar] [CrossRef]
- McCormick, A.J.; Cramer, M.D.; Watt, D.A. Changes in photosynthetic rates and gene expression of leaves during a source-sink perturbation in sugarcane. Ann. Bot. 2008, 101, 89–102. [Google Scholar] [CrossRef]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29, 15–21. [Google Scholar] [CrossRef]
- Kim, D.; Langmead, B.; Salzberg, S.L. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 2015, 12, 357–360. [Google Scholar] [CrossRef] [PubMed]
- Pertea, M.; Pertea, G.M.; Antonescu, C.M.; Chang, T.C.; Mendell, J.T.; Salzberg, S.L. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 2015, 33, 290–295. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed]
- Supek, F.; Bošnjak, M.; Škunca, N.; Šmuc, T. REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms. PLoS ONE 2011, 6, e21800. [Google Scholar] [CrossRef] [PubMed]
- Kanehisa, M.; Furumichi, M.; Sato, Y.; Kawashima, M.; Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2023, 51, D587–D592. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Jiao, C.; Sun, H.; Rosli, H.G.; Pombo, M.A.; Zhang, P.; Banf, M.; Dai, X.; Martin, G.B.; Giovannoni, J.J.; et al. iTAK: A Program for Genome-wide Prediction and Classification of Plant Transcription Factors, Transcriptional Regulators, and Protein Kinases. Mol. Plant 2016, 12, 1667–1670. [Google Scholar] [CrossRef]
- Chen, C.; Chen, H.; He, Y.; Xia, R. TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface. BioRxiv 2018, BioRxiv:289660. [Google Scholar] [CrossRef]
- Milligan, G.W.; Sokol, L.M. A Two-Stage Clustering Algorithm with Robust Recovery Characteristics. Educ. Psychol. Meas. 1980, 40, 755–759. [Google Scholar] [CrossRef]
- Saito, R.; Smoot, M.E.; Ono, K.; Ruscheinski, J.; Wang, P.L.; Lotia, S.; Pico, A.R.; Bader, G.D.; Ideker, T. A travel guide to Cytoscape plugins. Nat. Methods 2012, 9, 1069–1076. [Google Scholar] [CrossRef] [PubMed]
- Pan, X.; Welti, R.; Wang, X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat. Protoc. 2010, 5, 986–992. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; He, Y.; Wu, C.; Liu, H.; Hu, Z.; Sun, G. Cloning and Molecular Characterization of a SERK Gene Transcriptionally Induced During Somatic Embryogenesis in Ananas comosus cv. Shenwan. Plant Mol. Biol. Rep. 2012, 30, 195–203. [Google Scholar] [CrossRef]
- Ling, H.; Wu, Q.; Guo, J.; Xu, L.; Que, Y. Comprehensive selection of reference genes for gene expression normalization in sugarcane by real time quantitative RT-PCR. PLoS ONE 2014, 9, e97469. [Google Scholar] [CrossRef] [PubMed]
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Ain, N.-u.; Habiba; Ming, R. Allele-Specific Hormone Dynamics in Highly Transgressive F2 Biomass Segregants in Sugarcane (Saccharum spp.). Plants 2024, 13, 2247. https://doi.org/10.3390/plants13162247
Ain N-u, Habiba, Ming R. Allele-Specific Hormone Dynamics in Highly Transgressive F2 Biomass Segregants in Sugarcane (Saccharum spp.). Plants. 2024; 13(16):2247. https://doi.org/10.3390/plants13162247
Chicago/Turabian StyleAin, Noor-ul, Habiba, and Ray Ming. 2024. "Allele-Specific Hormone Dynamics in Highly Transgressive F2 Biomass Segregants in Sugarcane (Saccharum spp.)" Plants 13, no. 16: 2247. https://doi.org/10.3390/plants13162247