Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 11, 73

Comprehensive Expression Analysis Suggests Overlapping and Specific Roles of Rice Glutathione S-transferase Genes During Development and Stress Responses

Affiliations

Comprehensive Expression Analysis Suggests Overlapping and Specific Roles of Rice Glutathione S-transferase Genes During Development and Stress Responses

Mukesh Jain et al. BMC Genomics.

Abstract

Background: Glutathione S-transferases (GSTs) are the ubiquitous enzymes that play a key role in cellular detoxification. Although several GSTs have been identified and characterized in various plant species, the knowledge about their role in developmental processes and response to various stimuli is still very limited. In this study, we report genome-wide identification, characterization and comprehensive expression analysis of members of GST gene family in crop plant rice, to reveal their function(s).

Results: A systematic analysis revealed the presence of at least 79 GST genes in the rice genome. Phylogenetic analysis grouped GST proteins into seven classes. Sequence analysis together with the organization of putative motifs indicated the potential diverse functions of GST gene family members in rice. The tandem gene duplications have contributed a major role in expansion of this gene family. Microarray data analysis revealed tissue-/organ- and developmental stage-specific expression patterns of several rice GST genes. At least 31 GST genes showed response to plant hormones auxin and cytokinin. Furthermore, expression analysis showed the differential expression of quite a large number of GST genes during various abiotic stress (20), arsenate stress (32) and biotic stress (48) conditions. Many of the GST genes were commonly regulated by developmental processes, hormones, abiotic and biotic stresses.

Conclusion: The transcript profiling suggests overlapping and specific role(s) of GSTs during various stages of development in rice. Further, the study provides evidence for the role of GSTs in mediating crosstalk between various stress and hormone response pathways and represents a very useful resource for functional analysis of selected members of this family in rice.

Figures

Figure 1
Figure 1
Putative motifs predicted in rice GST proteins. Significant motifs (e-value <e-100) of more than 10 amino acid length present in at least 10 GST proteins were predicted by MEME search. The consensus sequence, length (amino acids), number of GST proteins containing the motif and e-value of each predicted motif is given. The first residue in motif 5 represents the active site serine residue.
Figure 2
Figure 2
Chromosomal distribution of rice GST genes. The chromosome number is indicated at the top of each chromosome. GST genes localized on duplicated chromosomal segments are connected by lines. The genes labeled on left side are oriented from bottom to top and those on right side are oriented from top to bottom on rice chromosomes. Six clusters (three on chromosome 1 and one each on chromosome 1, 10 and 12) of tandemly arranged GST genes are indicated in boxes. Exact position of each GST gene on rice chromosome pseudomolecules is given in Additional file 1.
Figure 3
Figure 3
Phylogenetic relationship among rice and Arabidopsis GST proteins and their classification. The unrooted tree was constructed based on multiple sequence alignment of full-length protein sequences using ClustalX program by neighbor-joining method with 1000 bootstrap replicates. The numbers at the nodes represent bootstrap values (≥ 500) from 1000 replicates. All the rice and Arabidopsis GST proteins grouped into seven classes. The bar indicates 0.1 substitutions per site. The cluster of Tau class GST genes present only in rice is indicated in box.
Figure 4
Figure 4
Expression patterns of rice GST genes in various tissues/organs and developmental stages. (A) Hierarchical clustering analysis of 71 GST genes represented on Affymetrix Rice Genome Array is shown. For clustering we used average log signal values for three biological replicates of each sample after normalization of the raw data (Additional file 6). The color scale for log signal values is shown at the bottom. Clusters (I-XVI) are marked on the right. ML, mature leaf; YL, Y-leaf; SAM, shoot apical meristem; P1-P6, stages of panicle development; S1-S5, stages of seed development. (B) Real-time PCR analysis of selected genes to validate their differential expression during various stages of development. The mRNA levels for each gene in different tissue samples were calculated relative to its expression in root. The error bars represent standard deviation. ML, mature leaf; YL, Y-leaf; SAM, shoot apical meristem; Stage 1-3 represent stages of panicle development (Stage 1 corresponds to P1 and P2; Stage 2, P3 and P4; Stage 3, P5 and P6); Stage 4 and 5 represent stages of seed development (Stage 4 corresponds to S1 and S2; Stage 5, S3-S5).
Figure 5
Figure 5
Expression patterns of representative duplicated GST genes in various tissues/organs and developmental stages. The average log signal values (from three biological replicates) for each gene in all the samples analyzed is presented on Y-axis. The expression patterns of all the duplicated GST genes in various tissues/organs and developmental stages is given in Additional file. ML, mature leaf; YL, Y-leaf; SAM, shoot apical meristem; P1-P6, stages of panicle development; S1-S5, stages of seed development.
Figure 6
Figure 6
Differential expression of rice GST genes in response to various abiotic and arsenate stress conditions. Hierarchical clustering of GST genes showing significant differential expression under at least one abiotic stress condition (A) or arsenate stress (B) is shown. The fold change values (Additional files 10, 11) in treated sample as compared to its corresponding mock-treated control sample were used for clustering. The color scale for fold change values is shown at the bottom. Venn diagram represents number of GST genes commonly or specifically regulated by various abiotic stress conditions. (C) Real-time PCR analysis of selected genes to validate their differential expression during various abiotic stress conditions. The mRNA levels for each gene in different tissue samples were calculated relative to its expression in control seedlings. The error bars represent standard deviation. DS, desiccation stress; SS, salt stress; CS, cold stress; ArS, arsenate stress. Azucena and Bala represent arsenate-sensitive and arsenate-resistant rice varieties, respectively.
Figure 7
Figure 7
Differential expression of rice GST genes in response to various biotic stress conditions. Hierarchical clustering of GST genes showing significant differential expression in at least one condition is shown. The fold change values (Additional file 12) in treated sample as compared to its corresponding mock-treated control sample were used for clustering. The color scale for fold change values is shown at the bottom. Dpi, days post-inoculation.
Figure 8
Figure 8
Venn diagram representing the number of GST genes commonly or specifically regulated by various environmental stimuli, including plant hormones, abiotic stress and/or biotic stress.

Similar articles

See all similar articles

Cited by 58 articles

See all "Cited by" articles

References

    1. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Ann Rev Pharmacol Toxicol. 2005;45:51–88. doi: 10.1146/annurev.pharmtox.45.120403.095857. - DOI - PubMed
    1. Sheehan D, Meade G, Foley VM, Dowd CA. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J. 2001;360:1–16. doi: 10.1042/0264-6021:3600001. - DOI - PMC - PubMed
    1. Pearson WR. Phylogenies of glutathione transferase families. Methods Enzymol. 2005;401:186–204. doi: 10.1016/S0076-6879(05)01012-8. - DOI - PubMed
    1. Pemble SE, Wardle AF, Taylor JB. Glutathione S-transferase class Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem J. 1996;319:749–754. - PMC - PubMed
    1. McGonigle B, Keeler SJ, Lau SM, Koeppe MK, O'Keefe DP. A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol. 2000;124:1105–1120. doi: 10.1104/pp.124.3.1105. - DOI - PMC - PubMed

Publication types

MeSH terms

LinkOut - more resources

Feedback