Integrative Transcriptomic Analysis Uncovers Novel Gene Modules That Underlie the Sulfate Response in

Overview

Journal Front Plant Sci

Date 2018 Apr 26

PMID 29692794

Citations 17

Authors

Carlos Henriquez-Valencia

Anita Arenas-M

Joaquin Medina

Javier Canales

Affiliations

Soon will be listed here.

Abstract

Sulfur is an essential nutrient for plant growth and development. Sulfur is a constituent of proteins, the plasma membrane and cell walls, among other important cellular components. To obtain new insights into the gene regulatory networks underlying the sulfate response, we performed an integrative meta-analysis of transcriptomic data from five different sulfate experiments available in public databases. This bioinformatic approach allowed us to identify a robust set of genes whose expression depends only on sulfate availability, indicating that those genes play an important role in the sulfate response. In relation to sulfate metabolism, the biological function of approximately 45% of these genes is currently unknown. Moreover, we found several consistent Gene Ontology terms related to biological processes that have not been extensively studied in the context of the sulfate response; these processes include cell wall organization, carbohydrate metabolism, nitrogen compound transport, and the regulation of proteolysis. Gene co-expression network analyses revealed relationships between the sulfate-responsive genes that were distributed among seven function-specific co-expression modules. The most connected genes in the sulfate co-expression network belong to a module related to the carbon response, suggesting that this biological function plays an important role in the control of the sulfate response. Temporal analyses of the network suggest that sulfate starvation generates a biphasic response, which involves that major changes in gene expression occur during both the early and late responses. Network analyses predicted that the sulfate response is regulated by a limited number of transcription factors, including MYBs, bZIPs, and NF-YAs. In conclusion, our analysis identified new candidate genes and provided new hypotheses to advance our understanding of the transcriptional regulation of sulfate metabolism in plants.

Citing Articles

Analysis of the quadruple lsu mutant reveals molecular determinants of the role of LSU proteins in sulfur assimilation in Arabidopsis.

Piotrowska J, Wawrzynska A, Olszak M, Krzyszton M, Apodiakou A, Alseekh S Plant J. 2024; 120(6):2919-2936.

PMID: 39612294 PMC: 11658185. DOI: 10.1111/tpj.17155.

Integrated Transcriptome Analysis Identified Key Expansin Genes Associated with Wheat Cell Wall, Grain Weight and Yield.

Mira J, Arenas-M A, Calderini D, Canales J Plants (Basel). 2023; 12(15).

PMID: 37571021 PMC: 10421294. DOI: 10.3390/plants12152868.

A Revised View of the Gene Family: New Functions in Plant Stress Responses and Phytohormone Signaling.

Canales J, Arenas-M A, Medina J, Vidal E Int J Mol Sci. 2023; 24(3).

PMID: 36769138 PMC: 9917515. DOI: 10.3390/ijms24032819.

Evolutionary and Gene Expression Analyses Reveal New Insights into the Role of Gene-Family in Plant Responses to Sulfate-Deficiency.

Uribe F, Henriquez-Valencia C, Arenas-M A, Medina J, Vidal E, Canales J Plants (Basel). 2022; 11(12).

PMID: 35736678 PMC: 9229004. DOI: 10.3390/plants11121526.

Local and Systemic Response to Heterogeneous Sulfate Resupply after Sulfur Deficiency in Rice.

Wang R, Liu L, Zhao F, Huang X Int J Mol Sci. 2022; 23(11).

PMID: 35682882 PMC: 9181796. DOI: 10.3390/ijms23116203.

References

Hubberten H, Klie S, Caldana C, Degenkolbe T, Willmitzer L, Hoefgen R . Additional role of O-acetylserine as a sulfur status-independent regulator during plant growth. Plant J. 2012; 70(4):666-77. DOI: 10.1111/j.1365-313X.2012.04905.x. View

Zhang Q, Wang J, Deng F, Yan Z, Xia Y, Wang Z . TqPCR: A Touchdown qPCR Assay with Significantly Improved Detection Sensitivity and Amplification Efficiency of SYBR Green qPCR. PLoS One. 2015; 10(7):e0132666. PMC: 4501803. DOI: 10.1371/journal.pone.0132666. View

Zhang J, Sun X, Zhang Z, Ni Y, Zhang Q, Liang X . Metabolite profiling of Arabidopsis seedlings in response to exogenous sinalbin and sulfur deficiency. Phytochemistry. 2011; 72(14-15):1767-78. DOI: 10.1016/j.phytochem.2011.06.002. View

Hirai M, Klein M, Fujikawa Y, Yano M, Goodenowe D, Yamazaki Y . Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem. 2005; 280(27):25590-5. DOI: 10.1074/jbc.M502332200. View

Wagner U, Edwards R, Dixon D, Mauch F . Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol. 2002; 49(5):515-32. DOI: 10.1023/a:1015557300450. View

Zhao H, Wu D, Kong F, Lin K, Zhang H, Li G . The Nuclear Factor Y Transcription Factors. Front Plant Sci. 2017; 7:2045. PMC: 5222873. DOI: 10.3389/fpls.2016.02045. View

Hoefgen R, Nikiforova V . Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant. 2008; 132(2):190-8. DOI: 10.1111/j.1399-3054.2007.01012.x. View

Zhang M, Hu X, Zhu M, Xu M, Wang L . Transcription factors NF-YA2 and NF-YA10 regulate leaf growth via auxin signaling in Arabidopsis. Sci Rep. 2017; 7(1):1395. PMC: 5431230. DOI: 10.1038/s41598-017-01475-z. View

Hirai M, Saito K . Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur deficiency. J Exp Bot. 2004; 55(404):1871-9. DOI: 10.1093/jxb/erh184. View

10.

Bhargava A, Clabaugh I, To J, Maxwell B, Chiang Y, Schaller G . Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013; 162(1):272-94. PMC: 3641208. DOI: 10.1104/pp.113.217026. View

11.

van Dam S, Vosa U, van der Graaf A, Franke L, de Magalhaes J . Gene co-expression analysis for functional classification and gene-disease predictions. Brief Bioinform. 2017; 19(4):575-592. PMC: 6054162. DOI: 10.1093/bib/bbw139. View

12.

Zrenner R, Riegler H, Marquard C, Lange P, Geserick C, Bartosz C . A functional analysis of the pyrimidine catabolic pathway in Arabidopsis. New Phytol. 2009; 183(1):117-132. PMC: 2713857. DOI: 10.1111/j.1469-8137.2009.02843.x. View

13.

Gutierrez R, Lejay L, Dean A, Chiaromonte F, Shasha D, Coruzzi G . Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol. 2007; 8(1):R7. PMC: 1839130. DOI: 10.1186/gb-2007-8-1-r7. View

14.

Yaffe H, Buxdorf K, Shapira I, Ein-Gedi S, Moyal-Ben Zvi M, Fridman E . LogSpin: a simple, economical and fast method for RNA isolation from infected or healthy plants and other eukaryotic tissues. BMC Res Notes. 2012; 5:45. PMC: 3282632. DOI: 10.1186/1756-0500-5-45. View

15.

Krouk G, Tranchina D, Lejay L, Cruikshank A, Shasha D, Coruzzi G . A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Comput Biol. 2009; 5(3):e1000326. PMC: 2652106. DOI: 10.1371/journal.pcbi.1000326. View

16.

Bielecka M, Watanabe M, Morcuende R, Scheible W, Hawkesford M, Hesse H . Transcriptome and metabolome analysis of plant sulfate starvation and resupply provides novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen and phosphorus nutritional responses in Arabidopsis. Front Plant Sci. 2015; 5:805. PMC: 4309162. DOI: 10.3389/fpls.2014.00805. View

17.

Romero L, Aroca M, Laureano-Marin A, Moreno I, Garcia I, Gotor C . Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant. 2013; 7(2):264-76. DOI: 10.1093/mp/sst168. View

18.

Dietrich K, Weltmeier F, Ehlert A, Weiste C, Stahl M, Harter K . Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell. 2011; 23(1):381-95. PMC: 3051235. DOI: 10.1105/tpc.110.075390. View

19.

Gigolashvili T, Kopriva S . Transporters in plant sulfur metabolism. Front Plant Sci. 2014; 5:442. PMC: 4158793. DOI: 10.3389/fpls.2014.00442. View

20.

Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P . Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell. 2004; 16(10):2693-704. PMC: 520965. DOI: 10.1105/tpc.104.023960. View