RNA interference of a putative S-adenosyl-L-homocysteine hydrolase gene affects larval performance in Leptinotarsa decemlineata (Say)
Graphical abstract
Introduction
Juvenile hormones (JHs) are a family of sesquiterpenoids, and regulate metamorphosis and reproduction in insects (Daimon et al., 2012, Noriega et al., 2006, Riddiford et al., 2013). JHs are produced and secreted from the corpora allata (CA), a pair of small endocrine organs just posterior to the brain (Riddiford, 2012, Riddiford et al., 2013). The biosynthetic pathway of JHs is conventionally divided into two main components, the early steps and the late steps (Belles et al., 2005). The early steps of JH biosynthesis follow the mevalonate pathway from acetyl-CoA to farnesyl pyrophosphate (FPP). During the late steps, FPP is first hydrolyzed to farnesol (Cao et al., 2009) and then oxidized successively to farnesal and farnesoic acid (FA) (Belles et al., 2005). FA is finally converted to the active JH by means of an epoxidation (C10, 11) and a methyl transfer (Marchal et al., 2010, Mayoral et al., 2009). The last two steps diverge depending on the insect order. In Lepidoptera, epoxidase may have higher affinity for FA, so FA is first epoxidized to JH acid, and then methylated to JH. In contrast, in insect species in Orthoptera, Diptera, Coleoptera and Dictyoptera, FA is first esterified to form methyl farnesoate (MF), and then MF was epoxidized to JH (Belles et al., 2005, Defelipe et al., 2011, Mayoral et al., 2009).
In insects, methylation of FA or JH acid using S-adenosyl-L-methionine (AdoMet) releases a byproduct S-adenosyl-L-homocysteine (AdoHcy) (Feyereisen and Farnsworth, 1987, Noriega et al., 2006, Tehlivets et al., 2013). AdoHcy inhibits a number of AdoMet-dependent methyltransferases in vitro, such as mammalian DNA (cytosine-5-)-methyltransferase, mRNA cap (guanine-N7-)-methyltransferase, tRNA (uracil-5-)-methyltransferase, protein isoprenylcysteine carboxylmethyltransferase and phospholipid methyltransferases (Bacolla et al., 1999, Baron and Casey, 2004, Hausmann et al., 2005, Mao et al., 1995), and in vivo, such as DNA (cytosine-5-)-methyltransferase and phospholipid methyltransferases (Castro et al., 2005, Malanovic et al., 2008). Rapid conversion of AdoHcy to adenosine and homocysteine prevents the feedback inhibition. AdoHcy hydrolase (SAHase, EC 3.3.1.1) is the only eukaryotic enzyme catabolizing AdoHcy (De La Haba and Cantoni, 1959, Luka et al., 2009). In the cockroach Diploptera punctata CAs, SAHase activity is high enough to rapidly hydrolyze AdoHcy and thus removes the inhibitory effect of AdoHcy on the methylation of FA (Feyereisen and Farnsworth, 1987). Accordingly, it can be hypothesized that SAHase is essential for JH biosynthesis in other insect species.
Leptinotarsa decemlineata (Say) is a notorious defoliator of potato, and often causes extremely large potato yield loss (Jiang et al., 2012). The beetle has a complicated and diverse life history (Alyokhin, 2009, Alyokhin et al., 2008). JH plays primary roles in the regulation of several most important events in the life cycle in L. decemlineata, including metamorphosis (Vermunt et al., 1999), reproduction (De Loof and De Wilde, 1970, Dortland, 1979, Lefevere and De Wilde, 1984) and diapause (De Loof and De Wilde, 1970, De Wilde and De Boer, 1969, Kramer, 1978, Lefevere and De Wilde, 1984, Schooneveld et al., 1977). Moreover, dietary ingestion of bacterially-expressed dsRNA can effectively knock down target genes in L. decemlineata (Zhu et al., 2011). Thus, L. decemlineata provides an excellent coleopteran model for studying the endocrine control of life history.
In the present paper, we first cloned a putative SAHase gene in L. decemlineata. We then studied the influence of bacterially-expressed LdSAHase dsRNA on the performance of the larvae. Since JH activity of pyriproxyfen has been proven in L. decemlineata (De Kort et al., 1997, Koopmanschap et al., 1989, Yi and Adams, 2000), we also tested the combined effect of pyriproxyfen and LdSAHase-dsRNA on the larvae. Our results support the hypothesis that SAHase plays a critical role in JH biosynthesis in insects.
Section snippets
Insect culture
Post-diapause L. decemlineata adults were collected from potato field in spring at Urumqi city (43.82N, 87.61E), Xinjiang Uygur autonomous region in China. Insects were routinely reared in an insectary according to a previously described method (Shi et al., 2013).
Molecular cloning
Total RNA was extracted from the 3rd-instar larvae using TRIzol reagent (Invitrogen) according to the manufacturer′s instructions, and was treated for 30 min at 37 °C with RNase free DNase I (Ambion, Austin, TX) to eliminate traces of
Identification of a putative LdSAHase
A cDNA of a putative SAHase containing the complete coding sequence was isolated from L. decemlineata. The cDNA consists of 1806 bp containing a 1575 bp protein-coding region. Its predicted protein has 525 amino acid residues, with a calculated molecular weight of 58.18 kDa and an isoelectric point of 7.46. The predicted protein is designated LdSAHase (Fig. S1). SAHase is an exceptionally well-conserved enzyme (Stepkowski et al., 2005). Of the SAHase-like proteins, LdSAHase shares great identities
Discussion
In JH biosynthesis pathway, methylation of farnesoic acid or JH acid using S-adenosyl-L-methionine generates a byproduct AdoHcy (Feyereisen and Farnsworth, 1987, Noriega et al., 2006, Tehlivets et al., 2013). It is hypothesized that rapid removal of AdoHcy is essential for JH biosynthesis in insect CA (Feyereisen and Farnsworth, 1987). SAHase is the only eukaryotic enzyme catabolizing AdoHcy (De La Haba and Cantoni, 1959, Luka et al., 2009). In the present paper, therefore, we cloned a putative
Acknowledgments
This research was supported by the National Natural Sciences Foundation of China (31272047) and a nationally special fund of China for agri-scientific research in the public interest (201103026). We are very grateful to Mr. Jiang He, Mrs. Wei-Hua Jiang, Mr. Zhi-Tian Wang, Mrs. Man-Hui Xiong, Mr. Wei-Ping Lu, and Mrs. Ping Liu for help in insect rearing and sample collection. We would like to thank other field entomologists and technicians at Urumqi city in Xinjiang Uygur autonomous region in
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