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Molecular Characterization, Mrna Expression and Alternative Splicing of Ryanodine Receptor Gene in the Brown Citrus Aphid, Toxoptera Citricida (Kirkaldy)

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Molecular Characterization, Mrna Expression and Alternative Splicing of Ryanodine Receptor Gene in the Brown Citrus Aphid, Toxoptera Citricida (Kirkaldy) Int. J. Mol. Sci. 2015, 16, 15220-15234; doi:10.3390/ijms160715220 OPEN ACCESS International Journal of Molecular Sciences ISSN 1422-0067 www.mdpi.com/journal/ijms Article Molecular Characterization, mRNA Expression and Alternative Splicing of Ryanodine Receptor Gene in the Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) Ke-Yi Wang, Xuan-Zhao Jiang, Guo-Rui Yuan, Feng Shang and Jin-Jun Wang * Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China; E-Mails: [email protected] (K.-Y.W.); [email protected] (X.-Z.J.); [email protected] (G.-R.Y.); [email protected] (F.S.) * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +86-23-6825-0255; Fax: +86-23-6825-1269. Academic Editor: Lee A. Bulla Received: 15 May 2015 / Accepted: 29 June 2015 / Published: 6 July 2015 Abstract: Ryanodine receptors (RyRs) play a critical role in regulating the release of intracellular calcium, which enables them to be effectively targeted by the two novel classes of insecticides, phthalic acid diamides and anthranilic diamides. However, less information is available about this target site in insects, although the sequence and structure information of target molecules are essential for designing new control agents of high selectivity and efficiency, as well as low non-target toxicity. Here, we provided sufficient information about the coding sequence and molecular structures of RyR in T. citricida (TciRyR), an economically important pest. The full-length TciRyR cDNA was characterized with an open reading frame of 15,306 nucleotides, encoding 5101 amino acid residues. TciRyR was predicted to embrace all the hallmarks of ryanodine receptor, typically as the conserved C-terminal domain with consensus calcium-biding EF-hands (calcium-binding motif) and six transmembrane domains, as well as a large N-terminal domain. qPCR analysis revealed that the highest mRNA expression levels of TciRyR were observed in the adults, especially in the heads. Alternative splicing in TciRyR was evidenced by an alternatively spliced exon, resulting from intron retention, which was different from the case of RyR in Myzus persicae characterized with no alternative splicing events. Diagnostic PCR analysis indicated that the splicing of this exon was not only regulated in a body-specific manner but also in a stage-dependent manner. Taken together, these results provide useful information for new insecticide design and further insights into the molecular basis of insecticide action. Int. J. Mol. Sci. 2015, 16 15221 Keywords: Toxoptera citricida; ryanodine receptor; mRNA expression; alternative splicing 1. Introduction Intracellular calcium (Ca2+) homeostasis is crucial for normal life activities because Ca2+ is a key second messenger that regulates a number of cellular processes, such as muscle contraction, hormone secretion, synaptic transmission, and gene transcription [1]. Ryanodine receptors (RyRs), also known as Ca2+ release channels, play an critical role in intracellular Ca2+ signaling by inducing the release of Ca2+ from the sarco/endoplasmic reticulum (SR/ER) lumen to the cytosol in muscle and non-muscle cells [2,3]. RyRs are homomeric tetramers with a total molecular mass higher than 2 MDa [4], composed of a hydrophilic domain at the N-terminus and a membrane-spanning domain at the C-terminus [5]. The N-terminal cytoplasmic domain, also known as the “foot structure”, is large and spans the junction between the transverse tubules and SR membranes. The C-terminal hydrophobic domain contains 4–12 transmembrane segments and forms the putative pore of the Ca2+ release channel [4,6]. In mammals, three RyR isoforms have been reported: RyR1, which is predominant in skeletal muscles, RyR2 is largely present in cardiac muscles, and RyR3, which is primarily present in the brain and diaphragm [6,7]. However, in birds, amphibians, and fish only two RyR isoforms (RyRA and RyRB), which are closely related to the mammalian RyR1 and RyR3, have been identified [8,9]. Unlike the vertebrates, insects are known to have only one RyR coding gene (Rya-r44F) [10], which shares about 45% sequence identity with either of the three mammalian RyRs [11]. Because the remarkable difference between the insects and mammalian RyRs could minimize the non-target effects on mammals, insect RyRs have been used as targets for insecticides, particularly phthalic acid diamides and anthranilic diamides [12,13]. These insecticides were previously known to be highly effective to lepidopteran pests [14], while recent researches indicate that these insecticides are also effective in controlling whiteflies and oriental fruit flies [15,16]. Hence, it is useful to estimate the toxicity of diamide insecticides to other insects in addition to lepidopteran pests, which will put forward the development of RyR targeting insecticides. In addition, the coding sequences of RyRs may provide key information to understand the molecular base that confers the high selectivity of these diamide insecticides. However, despite the increased availability of insect genomes, only 15 full-length insect RyR cDNAs have been cloned thus far. These RyRs are from insects including Drosophila melanogaster (DmRyR), Cnaphalocrocis medinalis (CmRyR), Nilaparvata lugens (NlRyR), Bemisia tabaci (BtRyR), Chilo suppressalis (CsRyR), Laodelphgax striatellus (LsRyR), Bactrocera dorsalis (BdRyR), Plutella xylostella (PxRyR), Ostrinia furnacalis (OfRyR), Helicoverpa armigera (HaRyR), Pieris rapae (PrRyR), Myzus persicae (MpRyR), Leptinotarsa decemlineata (LdRyR), Sogatella furcifera (SfRyR) and Tribolium castaneum (TcRyR) [10,17–28]. It is known that diamides activate insect RyRs, the resistance could result in gene mutations in RyRs [29]. For example, high levels of diamide cross-resistance P. xylostella strains collected from Philippines, Thailand, and China were found to be over 200-fold more resistant to chlorantraniliprole compared with susceptible strains; this resistance feature was associated with a mutation (G4946E) in the C-terminal membrane-spanning domain of PxRyR [30,31]. Three novel mutations including E1338D, Q4595L, and I4790M were Int. J. Mol. Sci. 2015, 16 15222 reported and displayed a significantly lower affinity to the chlorantraniliprole [32]. Hence, it is essential to obtain further insights into the molecular properties of insect RyRs. Due to the importance of RyRs as an insecticide target and limited information available about insect RyRs, we sequenced the coding region of RyR from the brown citrus aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae), an efficient vector of Citrus tristeza virus (CTV), which has now colonized virtually all of the world’s citrus production areas. Comparative analysis indicated that RyR in T. citricida (TciRyR) is functional and structural orthologs of insect RyRs. Moreover, we confirmed that TciRyR was product of alternative splicing suggesting that insect RyRs obtain functional diversity by generating alternative splicing variants. 2. Results 2.1. Cloning the Coding Sequence of Ryanodine Receptor (RyR) in Toxoptera citricida (TciRyR) A sequence of 15,639 bp was assembled from ten overlapping cDNA products (Figure 1), which covered the complete open reading frame (ORF) of 15,315 bp. The TciRyR (KP733849) ORF encoded a putative 5101-residues polypeptide, with a theoretical molecular weight of 580.08 kDa and PI (isoelectric point) of 5.49. Figure 1. Analysis of conserved structural domains in ryanodine receptor (RyR) and the strategy used to clone RyR in Toxoptera citricida (TciRyR). All fragments labeled “Tci” were used to assemble TciRyR. Lines show the length and relative location of amplicons. The location of putative transmembrane segments and conserved structural domains predicted by the Conserved Domains Database (NCBI) is shown. These include: MIR (protein mannosyltransferase, IP3R and RyR domain), RIH (RyR and IP3R homology), SPRY (spore lysisA and RyR domains), RyR (RyR domain), and RIH-associated (RyR and IP3R homology associated) domains, and EF-hands (calcium-binding motif) and transmembrane segments. Arrows indicate the location of alternatively spliced exon. 2.2. RyR Orthologs and Their Phylogeny All RyR orthologs deposited in GenBank were investigated by using the key words “Ryanodine receptor” and “RyR”. The results showed that RyR orthologs were widely distributed in Chordata, Int. J. Mol. Sci. 2015, 16 15223 Arthropoda, Nematoda, Platyhelminthes, Mollusca, Annelida, Echinodermata, Hemichordata, Placozoa, and Porifera, but not in Cnidaria, Protozoa, or Ctenophora. The Arthropoda orthologs with full-length cDNAs available were primarily found in Insecta, the majority of them are derived from Diptera, Lepidoptera, Hemiptera, Hymenoptera, and Coleoptera. Multiple protein alignments showed that TciRyR shared high similarity with the known insect RyRs. TciRyR shared the highest similarity with the RyRs from M. persicae (98.2%) and A. pisum (98.1%) at the protein level, 92.5% and 93.1% at the nucleotide level, respectively. The similarity between TciRyR with other insect orthologs ranged from 70% to 90%, such as 74.7% with DmRyR from D. melanogaster, 76.3% with AgRyR from A. gambiae, 77.7% with sRyR from B. mori and 81.1% with NlRyR from N. lugens. The similarity between TciRyR with the three RyRs isoforms of H. sapiens ranged from 43.0% to 46.0%. The phylogenetic analysis using the protein sequences of TciRyR and 53 other RyR homologs, including 36 insect RyRs
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