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

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.

Identifying Candidate Genes for Enhancing Grain Zn Concentration in Wheat

“…In Arabidopsis thaliana , the TFs bZIP19 and bZIP23 were shown to regulate the adaption to Zn deficiency in roots ( Assunção et al, 2010 ; Inaba et al, 2015 ). A total of 187 TabZIP genes have been identified in wheat ( Li et al, 2015 ) and a specific group of TabZIP genes conferred functional complementation of Zn deficiency-hypersensitive such as bzip19 bzip23 ( Evens et al, 2017 ; Henríquez-Valencia et al, 2018 ). So far, most functional studies of bZIPs were related to roots or leaves while little information about bZIP-dependent regulatory mechanisms is available for grains.…”

Central Role of Adenosine 5′-Phosphosulfate Reductase in the Control of Plant Hydrogen Sulfide Metabolism

“…The sulfur-responsive cis -element SURECOREATSULTR11 is sufficient and necessary for sulfur deficiency responsive expression of the high-affinity sulfate transporter gene SULTR1;1 in Arabidopsis roots, which could be reversed when supplied with cysteine and GSH ( Maruyama-Nakashita et al, 2005 ). APR3 (At4g21990) in Arabidopsis containing SURECOREATSULTR11 cis -acting element also shows response to sulfur deficiency conditions ( Maruyama-Nakashita et al, 2005 ; Henríquez-Valencia et al, 2018 ). However, although APR is highly regulated in plants, transcription factors responsible for this regulation are still not fully understood.…”

“…However, although APR is highly regulated in plants, transcription factors responsible for this regulation are still not fully understood. Bioinformatic approaches predict that gene expression response to sulfur deficiency is regulated by a limited number of transcription factors including MYBs, bZIPs, and NF-YAs, indicating that these transcription factors may play important roles in the sulfur status response ( Henríquez-Valencia et al, 2018 ). Besides, other cis -regulatory elements are found in the promoter region of SlAPR genes, which may response to distinct plant hormones, such as cytokinins, and several environmental factors, as well as CO 2 , light, and abiotic and biotic stresses.…”

Overexpression of the Selective Autophagy Cargo Receptor NBR1 Modifies Plant Response to Sulfur Deficit

“…During the last decades many research groups have been studying various aspects of plant response to sulfur deficit, and several reports on metabolome and transcriptome changes in plants starved for sulfur are available [11,12]. These experiments led not only to a demonstration of the linkage between the S, P and N nutrition, but they were also sufficient to identify the regulatory circuits involved in plant response to S nutrition status.…”