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Cyclic nucleotide-gated ion channel gene family in rice, identification, characterization and experimental analysis of expression response to plant hormones, biotic and abiotic stresses.

Nawaz Z, Kakar KU, Saand MA, Shu QY - BMC Genomics (2014)

Bottom Line: Gene duplication analysis revealed that both chromosomal segmentation (OsCNGC1 and 2, 10 and 11, 15 and 16) and tandem duplications (OsCNGC1 and 2) significantly contributed to the expansion of this gene family.We successively built a stringent motif: (LI-X(2)-[GS]-X-[FV]-X-G-[1]-ELL-X-W-X(12,22)-SA-X(2)-T-X(7)-[EQ]-AF-X-L) that recognizes the rice CNGCs specifically.The various cis-acting regulatory elements in the upstream sequences may be responsible for responding to multiple stimuli, including hormonal, biotic and abiotic stresses.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Rice Biology, Zhejiang University, Hangzhou 310029, China. qyshu@zju.edu.cn.

ABSTRACT

Background: Cyclic nucleotide-gated channels (CNGCs) are Ca2+-permeable cation transport channels, which are present in both animal and plant systems. They have been implicated in the uptake of both essential and toxic cations, Ca2+ signaling, pathogen defense, and thermotolerance in plants. To date there has not been a genome-wide overview of the CNGC gene family in any economically important crop, including rice (Oryza sativa L.). There is an urgent need for a thorough genome-wide analysis and experimental verification of this gene family in rice.

Results: In this study, a total of 16 full length rice CNGC genes distributed on chromosomes 1-6, 9 and 12, were identified by employing comprehensive bioinformatics analyses. Based on phylogeny, the family of OsCNGCs was classified into four major groups (I-IV) and two sub-groups (IV-A and IV- B). Likewise, the CNGCs from all plant lineages clustered into four groups (I-IV), where group II was conserved in all land plants. Gene duplication analysis revealed that both chromosomal segmentation (OsCNGC1 and 2, 10 and 11, 15 and 16) and tandem duplications (OsCNGC1 and 2) significantly contributed to the expansion of this gene family. Motif composition and protein sequence analysis revealed that the CNGC specific domain "cyclic nucleotide-binding domain (CNBD)" comprises a "phosphate binding cassette" (PBC) and a "hinge" region that is highly conserved among the OsCNGCs. In addition, OsCNGC proteins also contain various other functional motifs and post-translational modification sites. We successively built a stringent motif: (LI-X(2)-[GS]-X-[FV]-X-G-[1]-ELL-X-W-X(12,22)-SA-X(2)-T-X(7)-[EQ]-AF-X-L) that recognizes the rice CNGCs specifically. Prediction of cis-acting regulatory elements in 5' upstream sequences and expression analyses through quantitative qPCR demonstrated that OsCNGC genes were highly responsive to multiple stimuli including hormonal (abscisic acid, indoleacetic acid, kinetin and ethylene), biotic (Pseudomonas fuscovaginae and Xanthomonas oryzae pv. oryzae) and abiotic (cold) stress.

Conclusions: There are 16 CNGC genes in rice, which were probably expanded through chromosomal segmentation and tandem duplications and comprise a PBC and a "hinge" region in the CNBD domain, featured by a stringent motif. The various cis-acting regulatory elements in the upstream sequences may be responsible for responding to multiple stimuli, including hormonal, biotic and abiotic stresses.

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The maximum-likelihood (ML) phylogenetic tree ofCNGCfamily genes in 235 representative plant species. The rooted maximum-likelihood (ML) phylogenetic tree was inferred from the amino acid sequences alignment of full length proteins using MEGA 6.0, under the Jones-Taylor-Thornton (JTT) model. The bootstrap values from 1000 resampling, and cut-off values >70% are given at each node. The node color specifies group i.e. pink = I, light green = II-A, aqua = II-B, red = III, blue = IV-A, and black = IV-B. Rice CNGC genes are shown in blue color. Plant lineages are shown by shapes with different colors, i.e. green circle = dicots, maroon diamond = monocots, green diamond = gymnosperms, Aqua blue square = lycophytes, pink square = moss, and black triangles = green algae.
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Fig5: The maximum-likelihood (ML) phylogenetic tree ofCNGCfamily genes in 235 representative plant species. The rooted maximum-likelihood (ML) phylogenetic tree was inferred from the amino acid sequences alignment of full length proteins using MEGA 6.0, under the Jones-Taylor-Thornton (JTT) model. The bootstrap values from 1000 resampling, and cut-off values >70% are given at each node. The node color specifies group i.e. pink = I, light green = II-A, aqua = II-B, red = III, blue = IV-A, and black = IV-B. Rice CNGC genes are shown in blue color. Plant lineages are shown by shapes with different colors, i.e. green circle = dicots, maroon diamond = monocots, green diamond = gymnosperms, Aqua blue square = lycophytes, pink square = moss, and black triangles = green algae.

Mentions: A maximum likelihood tree was generated using amino acid sequences of the deduced full-length peptides with JTT (Jones, Taylor and Thornton) model. We used SYG1 from Saccharomyces cerevisiae as out-group [68]. According to the tree’s topology, CNGC gene family of all plant lineages clustered into four distinct groups (I-IV) with significant bootstrap values (Figure 5). Group II and group IV are subdivided into II-A/II-B and IV-A/IV-B. All the CNGCs from algae formed the basal lineage and clustered into same group (group VI-B), whereas those from the land plants grouped into several other groups (I–IV), showing that the CNGC family originated earlier than the separation of green algae and the ancestor of land plants. Among these four groups, only Group II was conserved in all land plants, showing that all CNGC genes from land plants shared a mutual ancestor after the divergence from aquatic plants. Group II-B was solely present in lower land plants including mosses (bryophytes) and lycophytes. Similarly, CNGCs from group I expanded in both mono- and dicotyledonous angiosperms, while group II-A and III was prevalent in all embryophytes (angiosperms and gymnosperms) (Figure 5). Group IV-A contain CNGCs from vascular plants i.e., embryophytes and lyophytes. These analyses revealed that all CNGC genes from land plants originated from a common ancestor, earlier than the split between lower and higher land plants [69], while the lineage specific expansion and divergence happened in higher land plants, particularly in dicots, after diversification from lower land plants, which lead to generation of group II-B in basal land plant and group I-IV in higher land plants. Moreover, CNGC genes from similar lineage, such as mosses, lycophytes, gymnosperms and angiosperms, inclined to be clustered together. Our interpretations are corroborated by the findings of previous studies [66, 68, 70, 71].Figure 5


Cyclic nucleotide-gated ion channel gene family in rice, identification, characterization and experimental analysis of expression response to plant hormones, biotic and abiotic stresses.

Nawaz Z, Kakar KU, Saand MA, Shu QY - BMC Genomics (2014)

The maximum-likelihood (ML) phylogenetic tree ofCNGCfamily genes in 235 representative plant species. The rooted maximum-likelihood (ML) phylogenetic tree was inferred from the amino acid sequences alignment of full length proteins using MEGA 6.0, under the Jones-Taylor-Thornton (JTT) model. The bootstrap values from 1000 resampling, and cut-off values >70% are given at each node. The node color specifies group i.e. pink = I, light green = II-A, aqua = II-B, red = III, blue = IV-A, and black = IV-B. Rice CNGC genes are shown in blue color. Plant lineages are shown by shapes with different colors, i.e. green circle = dicots, maroon diamond = monocots, green diamond = gymnosperms, Aqua blue square = lycophytes, pink square = moss, and black triangles = green algae.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4197254&req=5

Fig5: The maximum-likelihood (ML) phylogenetic tree ofCNGCfamily genes in 235 representative plant species. The rooted maximum-likelihood (ML) phylogenetic tree was inferred from the amino acid sequences alignment of full length proteins using MEGA 6.0, under the Jones-Taylor-Thornton (JTT) model. The bootstrap values from 1000 resampling, and cut-off values >70% are given at each node. The node color specifies group i.e. pink = I, light green = II-A, aqua = II-B, red = III, blue = IV-A, and black = IV-B. Rice CNGC genes are shown in blue color. Plant lineages are shown by shapes with different colors, i.e. green circle = dicots, maroon diamond = monocots, green diamond = gymnosperms, Aqua blue square = lycophytes, pink square = moss, and black triangles = green algae.
Mentions: A maximum likelihood tree was generated using amino acid sequences of the deduced full-length peptides with JTT (Jones, Taylor and Thornton) model. We used SYG1 from Saccharomyces cerevisiae as out-group [68]. According to the tree’s topology, CNGC gene family of all plant lineages clustered into four distinct groups (I-IV) with significant bootstrap values (Figure 5). Group II and group IV are subdivided into II-A/II-B and IV-A/IV-B. All the CNGCs from algae formed the basal lineage and clustered into same group (group VI-B), whereas those from the land plants grouped into several other groups (I–IV), showing that the CNGC family originated earlier than the separation of green algae and the ancestor of land plants. Among these four groups, only Group II was conserved in all land plants, showing that all CNGC genes from land plants shared a mutual ancestor after the divergence from aquatic plants. Group II-B was solely present in lower land plants including mosses (bryophytes) and lycophytes. Similarly, CNGCs from group I expanded in both mono- and dicotyledonous angiosperms, while group II-A and III was prevalent in all embryophytes (angiosperms and gymnosperms) (Figure 5). Group IV-A contain CNGCs from vascular plants i.e., embryophytes and lyophytes. These analyses revealed that all CNGC genes from land plants originated from a common ancestor, earlier than the split between lower and higher land plants [69], while the lineage specific expansion and divergence happened in higher land plants, particularly in dicots, after diversification from lower land plants, which lead to generation of group II-B in basal land plant and group I-IV in higher land plants. Moreover, CNGC genes from similar lineage, such as mosses, lycophytes, gymnosperms and angiosperms, inclined to be clustered together. Our interpretations are corroborated by the findings of previous studies [66, 68, 70, 71].Figure 5

Bottom Line: Gene duplication analysis revealed that both chromosomal segmentation (OsCNGC1 and 2, 10 and 11, 15 and 16) and tandem duplications (OsCNGC1 and 2) significantly contributed to the expansion of this gene family.We successively built a stringent motif: (LI-X(2)-[GS]-X-[FV]-X-G-[1]-ELL-X-W-X(12,22)-SA-X(2)-T-X(7)-[EQ]-AF-X-L) that recognizes the rice CNGCs specifically.The various cis-acting regulatory elements in the upstream sequences may be responsible for responding to multiple stimuli, including hormonal, biotic and abiotic stresses.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Rice Biology, Zhejiang University, Hangzhou 310029, China. qyshu@zju.edu.cn.

ABSTRACT

Background: Cyclic nucleotide-gated channels (CNGCs) are Ca2+-permeable cation transport channels, which are present in both animal and plant systems. They have been implicated in the uptake of both essential and toxic cations, Ca2+ signaling, pathogen defense, and thermotolerance in plants. To date there has not been a genome-wide overview of the CNGC gene family in any economically important crop, including rice (Oryza sativa L.). There is an urgent need for a thorough genome-wide analysis and experimental verification of this gene family in rice.

Results: In this study, a total of 16 full length rice CNGC genes distributed on chromosomes 1-6, 9 and 12, were identified by employing comprehensive bioinformatics analyses. Based on phylogeny, the family of OsCNGCs was classified into four major groups (I-IV) and two sub-groups (IV-A and IV- B). Likewise, the CNGCs from all plant lineages clustered into four groups (I-IV), where group II was conserved in all land plants. Gene duplication analysis revealed that both chromosomal segmentation (OsCNGC1 and 2, 10 and 11, 15 and 16) and tandem duplications (OsCNGC1 and 2) significantly contributed to the expansion of this gene family. Motif composition and protein sequence analysis revealed that the CNGC specific domain "cyclic nucleotide-binding domain (CNBD)" comprises a "phosphate binding cassette" (PBC) and a "hinge" region that is highly conserved among the OsCNGCs. In addition, OsCNGC proteins also contain various other functional motifs and post-translational modification sites. We successively built a stringent motif: (LI-X(2)-[GS]-X-[FV]-X-G-[1]-ELL-X-W-X(12,22)-SA-X(2)-T-X(7)-[EQ]-AF-X-L) that recognizes the rice CNGCs specifically. Prediction of cis-acting regulatory elements in 5' upstream sequences and expression analyses through quantitative qPCR demonstrated that OsCNGC genes were highly responsive to multiple stimuli including hormonal (abscisic acid, indoleacetic acid, kinetin and ethylene), biotic (Pseudomonas fuscovaginae and Xanthomonas oryzae pv. oryzae) and abiotic (cold) stress.

Conclusions: There are 16 CNGC genes in rice, which were probably expanded through chromosomal segmentation and tandem duplications and comprise a PBC and a "hinge" region in the CNBD domain, featured by a stringent motif. The various cis-acting regulatory elements in the upstream sequences may be responsible for responding to multiple stimuli, including hormonal, biotic and abiotic stresses.

Show MeSH