2023, Issue 5, Volume 15

RELATIONSHIP BETWEEN TFBS ABUNDANCE AND GENE EXPRESSION IN CARBOHYDRATE METABOLISM-RELATED GENES DURING FLOWERING IN RICE

M. Krishna Kumar+, D.P. Syamaladevi*, S.M. Balachandran and D. Subrahmanyan

ICAR-Indian Institute of Rice Research, Hyderabad, India. PIN 500 030

£ Currently at: ICAR-Indian Institute of Spices Research, Kozhikode

Email: dpsdevi@gmail.com

Received-01.05.2023, Revised-12.05.2023, Accepted-23.05.2023

Abstract: The abundance of transcription factor binding sites (TFBSs) on promoter sequences differs from gene to gene. Understanding how this difference affects gene expression would enable us to develop superior lines through allele mining based genomic selection or genome editing. To understand the relationship between the TFBSs abundance and transcription in carbohydrate metabolism-related genes that are central to growth and grain yield in rice. For this, we first analysed the expression pattern of four carbohydrate metabolism-related enzymes – Sucrose Phosphate Synthase (SPS), PME (Pectin Methyl Esterase), Galacturonosyl transferase (GalAT) and Phosphoglucomutase (PGM). Then, we obtained a reliable set of TFBSs on the core and distal promoters of these genes following Support Vector Machine (SVM) method and stringent cut off of 90% TFBS motif similarity. Fold change in gene expression during phenology change from vegetative to flowering showed a linear relationship with the TFBS abundance in the case of an SBP family transcription factor, SPL12. Further, identification of CpG islands in the promoters explained the deviations in this linear relationship between gene expression and TFBS abundance. Using two DNA parameters – the TFBS abundance and the CpG islands – we provide predictive insights to the gene expression of carbohydrate metabolism-related genes in rice.

Keywords: Transcription factor binding sites, Gene expression, Carbohydrate metabolism, Phosphoglucomutase, Rice

References

Bahaji et al. (2015). Plastidic phosphoglucose isomerase is an important determinant of starch accumulation in mesophyll cells, growth, photosynthetic capacity, and biosynthesis of plastidic cytokinins in Arabidopsis PLoS ONE 10(3), e0119641.

Google Scholar

Ballare et al. (2013). Nucleosome-driven transcription factor binding and gene regulation. Molecular Cell, 49, 67–79.

Google Scholar

Bosch et al (2005) Pectin methyl esterases and pectin dynamics in pollen tubes. Plant Cell, 17(12), 3219–3226.

Google Scholar

Brignall et al. ( 2019) Considering abundance, affinity, and binding site availability in the nf-κb target selection puzzle. Frontiers in immunology, 10:609.

Google Scholar

Bruneau et al. (1991) Sucrose phosphate synthase, a key enzyme for sucrose biosynthesis in plants: protein purification from corn leaves and immunological detection. Plant Physiol., 96(2), 473–478.

Google Scholar

Cao and Jacobsen (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyl transferase genes. Proc Natl Acad Sci USA, 99, 16491–16498.

Google Scholar

Chang et al. (2008) PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups BMC. Genomics, 9, 561.

Google Scholar

Chomczynski, P. and Mackey, K. (1995) Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources, Biotechniques,19(6), 942-5.

Google Scholar

Chow et al. (2019) PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Res., 47, D1155–D1163.

Google Scholar

Daynard et al. (1969) Contribution of stalk soluble carbohydrates to grain yield in corn (Zea mays L.). Crop Sci., 9, 831–834.

Google Scholar

Deng et al. (2016) Polyaspartate urea and nitrogen management affect nonstructural carbohydrates and yield of rice. Crop Sci., 56, 3272–3285.

Google Scholar

Egli et al. (2010) Loss of cytosolic  phospho-glucomutase compromises gametophyte development in Arabidopsis. Plant Physiology, 154, 659–1671.

Google Scholar

Fu et al. (2011) Pre-anthesis non-structural carbohydrate reserve in the stem enhances the sink strength of inferior spikelets during grain filling of rice. Field Crops Res.,123, 170–182.

Google Scholar

Fujita et al. (2010) Rice expression atlas in reproductive development. Plant and Cell Physiology, 51(12), 2060–2081.

Google Scholar

Gebbing and Schnyder (1999) Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat. Plant Physiol. 121, 871–878.

Google Scholar

Godoy et al. (2013) Galacturonosyltransferase 4 silencing alters pectin composition and carbon partitioning in tomato. Journal of Experimental Botany, 64(8), 2449–2466.

Google Scholar

Hofhuis and Heidstra (2018) Transcription factor dosage: more or less sufficient for growth Current Opinion in Plant Biology 45(A), 50-58.

Google Scholar

Jeske et al (2019) BRENDA in 2019: a European ELIXIR core data resource. Nucleic Acids Res., 47(D1), D542-D549.

Google Scholar

Johnson et al. (2007) Genome-wide mapping of in vivo protein-DNA interactions Science, 316, 1497–1502. 

Google Scholar

Kobayashi et al. (2010) The spatial expression and regulation of transcription factors IDEF1 and IDEF2. Ann Bot., 105(7), 1109–1117.

Google Scholar

Kobayashi et al. (2007) The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants Proceedings of the National Academy of Sciences, 104(48), 19150-19155.

Google Scholar

Kanehisa and Goto (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes Nucleic Acids Res., 28, 27-30.

Google Scholar

Li et al. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance Plant Cell 20(8), 2238-51.

Google Scholar

Li et al. (2015) The Arabidopsis thaliana TCP transcription factors: A broadening horizon beyond development Plant Signal Behav 10(7), e1044192.

Google Scholar

Lindroth et al. (2001) Requirement of Chromomethylase3 for maintenance of CpXpG methylation. Science, 292, 2077–2080.

Google Scholar

Louvet et al. (2006)  Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta, 224(4), 782-91.

Google Scholar

Luu et al. (2013) Disclosing the crosstalk among DNA methylation, transcription factors, and histone marks in human pluripotent cells through discovery of DNA methylation motifs. Genome Res., 23, 2013-2029.

Google Scholar

Malinova et al. (2014) Reduction of the cytosolic Phosphoglucomutase in Arabidopsis reveals impact on plant growth, seed and root development, and carbohydrate partitioning PLoS ONE 9(11): e112468. 

Google Scholar

Mikkelsen et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature448, 553–560. 

Google Scholar

Ogo et al. (2008) A Novel NAC Transcription Factor, IDEF2, That Recognizes the Iron Deficiency-responsive Element 2 Regulates the Genes Involved in Iron Homeostasis in Plants. Journal of Biological Chemistry, 283(19), 13407-17.

Google Scholar

Orfila et al (2005) QUASIMODO1 is expressed in vascular tissue of Arabidopsis thaliana inflorescence stems, and affects homogalacturonan and xylan biosynthesis. Planta222, 613–622.

Google Scholar

Peaucelle et al (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol., 21, 1720–1726.

Google Scholar

Ponger and Mouchiroud (2002) CpGProD: identifying CpG islands associated with transcription start sites in large genomic mammalian sequences. Bioinformatics, 18 (4), 631-633.

Google Scholar

Pradhan et al (1999) Effect of CWG methylation on expression of plant genes. Biochem J. 341, 473–476.

Google Scholar

Proseus et al (2006) Calcium pectate chemistry controls growth rate of Characorallina. Journal of experimental botany, 57(15), 3989–4002.

Google Scholar

Robertson et al (2007) Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods, 4, 651–657.

Google Scholar

Rozenberg et al (2008) All and only CpG containing sequences are enriched in promoters abundantly bound by RNA polymerase II in multiple tissues BMC Genomics, 9, 67.

Google Scholar

Sakai et al (2013) Rice Annotation Project Database (RAP-DB): An integrative and interactive database for rice genomics. Plant & Cell Physiol., 54(2):e6.

Google Scholar

Seong et al (2013) Transient overexpression of the Miscanthussinensis glucose-6-phosphate isomerase gene (MsGPI) in Nicotianabenthamiana enhances expression of genes related to antioxidant metabolism POJ 6(6), 408-414.

Google Scholar

Shikata et al (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol., 50(12), 2133-45.

Google Scholar

Sterling et al (2006) Functional identification of an Arabidopsis pectin biosynthetic homogalacturo nangalacturonosyl transferase Proceedings of the National Academy of Sciences, USA 103, 5236–5241.

Google Scholar

Suzuki and Bird (2008) DNA methylation landscapes: Provocative insights from epigenomics. Nature Reviews Genetics, 9, 465–476.

Google Scholar

Wang et al (2016) Squamosa promoter binding Protein-Like 2 controls floral organ development and plant fertility by activating ASYMMETRIC LEAVES 2 in Arabidopsis thaliana. Plant Mol Biol 92(6), 661-674.

Google Scholar

Wang et al (2013) Arabidopsis Galacturonosyl transferase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth. Molecular Plant, 6(4), 1131-1148.

Google Scholar

Wen et al (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell, 11, 1129–1140.

Google Scholar

Xu et al (2016) Developmental functions of miR156-regulated Squamosa Promoter binding protein-like (spl) Genes in Arabidopsis thaliana PLoS Genet 12(8), e1006263.

Google Scholar