Limits...
Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice.

Oono Y, Yazawa T, Kawahara Y, Kanamori H, Kobayashi F, Sasaki H, Mori S, Wu J, Handa H, Itoh T, Matsumoto T - PLoS ONE (2014)

Bottom Line: Plant growth is severely affected by toxic concentrations of the non-essential heavy metal cadmium (Cd).In this study, rice plants were hydroponically treated with 50 µM Cd for 24 hours and ∼60,000 expressed transcripts, including transcripts that could not be characterized by microarray-based approaches, were evaluated.Furthermore, qRT-PCR analyses of randomly selected Cd-responsive metal transporter transcripts under various metal ion stresses suggested that the expression of Cd-responsive transcripts might be easily affected by other ions.

View Article: PubMed Central - PubMed

Affiliation: Agrogenomics Research Center, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.

ABSTRACT
Plant growth is severely affected by toxic concentrations of the non-essential heavy metal cadmium (Cd). Comprehensive transcriptome analysis by RNA-Seq following cadmium exposure is required to further understand plant responses to Cd and facilitate future systems-based analyses of the underlying regulatory networks. In this study, rice plants were hydroponically treated with 50 µM Cd for 24 hours and ∼60,000 expressed transcripts, including transcripts that could not be characterized by microarray-based approaches, were evaluated. Upregulation of various ROS-scavenging enzymes, chelators and metal transporters demonstrated the appropriate expression profiles to Cd exposure. Gene Ontology enrichment analysis of the responsive transcripts indicated the upregulation of many drought stress-related genes under Cd exposure. Further investigation into the expression of drought stress marker genes such as DREB suggested that expression of genes in several drought stress signal pathways was activated under Cd exposure. Furthermore, qRT-PCR analyses of randomly selected Cd-responsive metal transporter transcripts under various metal ion stresses suggested that the expression of Cd-responsive transcripts might be easily affected by other ions. Our transcriptome analysis demonstrated a new transcriptional network linking Cd and drought stresses in rice. Considering our data and that Cd is a non-essential metal, the network underlying Cd stress responses and tolerance, which plants have developed to adapt to other stresses, could help to acclimate to Cd exposure. Our examination of this transcriptional network provides useful information for further studies of the molecular mechanisms of plant adaptation to Cd exposure and the improvement of tolerance in crop species.

Show MeSH

Related in: MedlinePlus

Relative expression of transcripts that may function in defense and detoxification under Cd treatment.RPKM fold changes at 1 h and 24 h were calculated for Cd treated samples compared with non-treated samples (0 h). (A) Relative expression of the GST gene family, (B) the Prx gene family, and (C) the MT gene family are shown. The x-axis shows transcripts and y-axis shows relative expression. The black bar shows the relative expression in roots at 1 h, the red bar roots at 24 h, the light blue bar shoots at 1 h and the blue bar shoots at 24 h.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4016200&req=5

pone-0096946-g004: Relative expression of transcripts that may function in defense and detoxification under Cd treatment.RPKM fold changes at 1 h and 24 h were calculated for Cd treated samples compared with non-treated samples (0 h). (A) Relative expression of the GST gene family, (B) the Prx gene family, and (C) the MT gene family are shown. The x-axis shows transcripts and y-axis shows relative expression. The black bar shows the relative expression in roots at 1 h, the red bar roots at 24 h, the light blue bar shoots at 1 h and the blue bar shoots at 24 h.

Mentions: The production of ROS is unavoidable under various biotic and abiotic stresses including Cd exposure. The accumulation of ROS is largely counteracted by an intricate antioxidant defense system [6]. The enzymatic scavengers GST [65] (Pfam accession: PF02798.15, PF13417.1, PF13410.1, PF00043.20, http://pfam.sanger.ac.uk/) and class III Peroxidase (Prx) (E.C. 1.11.1.7) [66] have large and complex gene families that control key metabolic steps in many eukaryotic systems. Among 80 GST genes, the responsive genes tended to be more upregulated in roots at 24 h compared with the other tissue/treatment combinations. In particular, GSTU12 (shoot), GSTU19 (root and shoot), GSTU24 (root and shoot), GSTU30 (shoot), GSTU31 (root) and GSTU39 (root) were strongly upregulated [fold change (FC) > 20] (Figure 4A). GSTU19, GSTU24 and GSTU39 were found to be upregulated in the roots of rice seedlings under arsenate exposure using a microarray platform [67], suggesting that part of the Cd defense might be similar to the As defense in the roots of rice. Enhanced GST with glutathione peroxidase activity in transgenic tobacco increased glutathione-dependent peroxide scavenging and alterations in glutathione and ascorbate metabolism that led to reduced oxidative damage [68]. Class III Prx genes catalyze the reduction of H2O2 by transferring electrons to various donor molecules such as lignin precursors and secondary metabolites [69], [70]. Prx22, Prx59, Prx62, Prx86, Prx110, Prx111 and Prx131 among 138 Prxs were upregulated strongly (FC > 20) in shoots after 24 h of Cd exposure (Figure 4A). Prx86 and Prx111 were strongly upregulated in the plant defense against a gall midge [71] and against Xanthomonas oryzae and Magnaporthe grisea[72]. As many studies have described the diverse functions of Prx in Arabidopsis[8], [73], these genes might be expressed in a time and tissue specific manner in rice.


Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice.

Oono Y, Yazawa T, Kawahara Y, Kanamori H, Kobayashi F, Sasaki H, Mori S, Wu J, Handa H, Itoh T, Matsumoto T - PLoS ONE (2014)

Relative expression of transcripts that may function in defense and detoxification under Cd treatment.RPKM fold changes at 1 h and 24 h were calculated for Cd treated samples compared with non-treated samples (0 h). (A) Relative expression of the GST gene family, (B) the Prx gene family, and (C) the MT gene family are shown. The x-axis shows transcripts and y-axis shows relative expression. The black bar shows the relative expression in roots at 1 h, the red bar roots at 24 h, the light blue bar shoots at 1 h and the blue bar shoots at 24 h.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4016200&req=5

pone-0096946-g004: Relative expression of transcripts that may function in defense and detoxification under Cd treatment.RPKM fold changes at 1 h and 24 h were calculated for Cd treated samples compared with non-treated samples (0 h). (A) Relative expression of the GST gene family, (B) the Prx gene family, and (C) the MT gene family are shown. The x-axis shows transcripts and y-axis shows relative expression. The black bar shows the relative expression in roots at 1 h, the red bar roots at 24 h, the light blue bar shoots at 1 h and the blue bar shoots at 24 h.
Mentions: The production of ROS is unavoidable under various biotic and abiotic stresses including Cd exposure. The accumulation of ROS is largely counteracted by an intricate antioxidant defense system [6]. The enzymatic scavengers GST [65] (Pfam accession: PF02798.15, PF13417.1, PF13410.1, PF00043.20, http://pfam.sanger.ac.uk/) and class III Peroxidase (Prx) (E.C. 1.11.1.7) [66] have large and complex gene families that control key metabolic steps in many eukaryotic systems. Among 80 GST genes, the responsive genes tended to be more upregulated in roots at 24 h compared with the other tissue/treatment combinations. In particular, GSTU12 (shoot), GSTU19 (root and shoot), GSTU24 (root and shoot), GSTU30 (shoot), GSTU31 (root) and GSTU39 (root) were strongly upregulated [fold change (FC) > 20] (Figure 4A). GSTU19, GSTU24 and GSTU39 were found to be upregulated in the roots of rice seedlings under arsenate exposure using a microarray platform [67], suggesting that part of the Cd defense might be similar to the As defense in the roots of rice. Enhanced GST with glutathione peroxidase activity in transgenic tobacco increased glutathione-dependent peroxide scavenging and alterations in glutathione and ascorbate metabolism that led to reduced oxidative damage [68]. Class III Prx genes catalyze the reduction of H2O2 by transferring electrons to various donor molecules such as lignin precursors and secondary metabolites [69], [70]. Prx22, Prx59, Prx62, Prx86, Prx110, Prx111 and Prx131 among 138 Prxs were upregulated strongly (FC > 20) in shoots after 24 h of Cd exposure (Figure 4A). Prx86 and Prx111 were strongly upregulated in the plant defense against a gall midge [71] and against Xanthomonas oryzae and Magnaporthe grisea[72]. As many studies have described the diverse functions of Prx in Arabidopsis[8], [73], these genes might be expressed in a time and tissue specific manner in rice.

Bottom Line: Plant growth is severely affected by toxic concentrations of the non-essential heavy metal cadmium (Cd).In this study, rice plants were hydroponically treated with 50 µM Cd for 24 hours and ∼60,000 expressed transcripts, including transcripts that could not be characterized by microarray-based approaches, were evaluated.Furthermore, qRT-PCR analyses of randomly selected Cd-responsive metal transporter transcripts under various metal ion stresses suggested that the expression of Cd-responsive transcripts might be easily affected by other ions.

View Article: PubMed Central - PubMed

Affiliation: Agrogenomics Research Center, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki, Japan.

ABSTRACT
Plant growth is severely affected by toxic concentrations of the non-essential heavy metal cadmium (Cd). Comprehensive transcriptome analysis by RNA-Seq following cadmium exposure is required to further understand plant responses to Cd and facilitate future systems-based analyses of the underlying regulatory networks. In this study, rice plants were hydroponically treated with 50 µM Cd for 24 hours and ∼60,000 expressed transcripts, including transcripts that could not be characterized by microarray-based approaches, were evaluated. Upregulation of various ROS-scavenging enzymes, chelators and metal transporters demonstrated the appropriate expression profiles to Cd exposure. Gene Ontology enrichment analysis of the responsive transcripts indicated the upregulation of many drought stress-related genes under Cd exposure. Further investigation into the expression of drought stress marker genes such as DREB suggested that expression of genes in several drought stress signal pathways was activated under Cd exposure. Furthermore, qRT-PCR analyses of randomly selected Cd-responsive metal transporter transcripts under various metal ion stresses suggested that the expression of Cd-responsive transcripts might be easily affected by other ions. Our transcriptome analysis demonstrated a new transcriptional network linking Cd and drought stresses in rice. Considering our data and that Cd is a non-essential metal, the network underlying Cd stress responses and tolerance, which plants have developed to adapt to other stresses, could help to acclimate to Cd exposure. Our examination of this transcriptional network provides useful information for further studies of the molecular mechanisms of plant adaptation to Cd exposure and the improvement of tolerance in crop species.

Show MeSH
Related in: MedlinePlus