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How Did Arthropod Sesquiterpenoids and Ecdysteroids Arise? Comparison of Hormonal Pathway Genes in Noninsect Arthropod Genomes.

Qu Z, Kenny NJ, Lam HM, Chan TF, Chu KH, Bendena WG, Tobe SS, Hui JH - Genome Biol Evol (2015)

Bottom Line: Moreover, we found that the "Broad-Complex" was specifically gained in the Pancrustacea, and the innovation of juvenile hormone (JH) in the insect linage correlates with the gain of the JH epoxidase (CYP15A1/C1) and the key residue changes in the binding domain of JH receptor ("Methoprene-tolerant").Furthermore, the gain of "Phantom" differentiates chelicerates from the other arthropods in using ponasterone A rather than 20-hydroxyecdysone as molting hormone.This study establishes a comprehensive framework for interpreting the evolution of these vital hormonal pathways in these most successful animals, the arthropods, for the first time.

View Article: PubMed Central - PubMed

Affiliation: Simon F.S. Li Marine Science Laboratory of School of Life Sciences and Center for Soybean Research of Partner State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong.

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— Schematic diagrams showing (A) biosynthetic and (B) degradative pathways of sesquiterpenoid hormones in arthropods (Hui et al 2010, 2013; Sin et al 2014; for details, refer to the main text); (C) summary of the presence of the sesquiterpenoid biosynthetic, degradative, and signaling pathway genes in the investigated arthropod genomes. “+” denotes presence and “−” represents the absence of supporting evidence.
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evv120-F1: — Schematic diagrams showing (A) biosynthetic and (B) degradative pathways of sesquiterpenoid hormones in arthropods (Hui et al 2010, 2013; Sin et al 2014; for details, refer to the main text); (C) summary of the presence of the sesquiterpenoid biosynthetic, degradative, and signaling pathway genes in the investigated arthropod genomes. “+” denotes presence and “−” represents the absence of supporting evidence.

Mentions: Sesquiterpenoids are a class of hydrocarbon/terpenes found in arthropods and plants; in arthropods, they are derived from the conversion of acetate via the mevalonate pathway (Tobe and Bendena 1999; Belles et al. 2005; Hui et al. 2010, 2013). In insects, there are two alternative pathways for the biosynthesis of JH: Either through the conversion of farnesoic acid (FA) to JH-III acid (JHA) by an epoxidase (CYP15C1) followed by methylation by JH acid methyltransferase (JHAMT) in the lepidopterans; or methylation of FA to MF by JHAMT followed by oxidation by another epoxidase (e.g., CYP15A1) as found in cockroaches and locust (Helvig et al. 2004; Belles et al. 2005; Marchal et al. 2011; Daimon et al. 2012; fig. 1A). In crustaceans, MF is synthesized through methylation of FA (Tobe et al. 1989). In addition to playing defensive roles in some social insects such as ants and bees, sesquiterpenoids including MF and JH are endogenously produced as master controllers of molting and sexual maturity in crustaceans and insects, respectively (Nagaraju 2007; Riddiford 2008). Although JH has never been identified in noninsect arthropods, JH mimics have been observed to play a role in controlling sex development and predator response in D. pulex (Olmstead and Leblanc 2002; Tatarazako et al. 2003; Miyakawa, Gotoh, et al. 2013). Recently, it has also been noted that the genes involved in JH production and degradation pathways, previously thought to be insect specific, are identified in water flea, shrimp, and centipede (Chipman et al. 2014; Sin et al. 2014). Here, we have identified JHAMT orthologs in the genomes of all investigated arthropods (fig. 1C and supplementary figs. S1 and S20, Supplementary Material online), suggesting the existence of a sesquiterpenoid biosynthetic system in the last common ancestor of all arthropods. However, no homologs of insect JH epoxidase (CYP15A1 or C1) could be identified in any of these noninsect arthropod genomes (fig. 1C). On the basis of this finding, we conclude, for the first time, that JH epoxidase was specifically gained in the insect lineage.Fig. 1.


How Did Arthropod Sesquiterpenoids and Ecdysteroids Arise? Comparison of Hormonal Pathway Genes in Noninsect Arthropod Genomes.

Qu Z, Kenny NJ, Lam HM, Chan TF, Chu KH, Bendena WG, Tobe SS, Hui JH - Genome Biol Evol (2015)

— Schematic diagrams showing (A) biosynthetic and (B) degradative pathways of sesquiterpenoid hormones in arthropods (Hui et al 2010, 2013; Sin et al 2014; for details, refer to the main text); (C) summary of the presence of the sesquiterpenoid biosynthetic, degradative, and signaling pathway genes in the investigated arthropod genomes. “+” denotes presence and “−” represents the absence of supporting evidence.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4524487&req=5

evv120-F1: — Schematic diagrams showing (A) biosynthetic and (B) degradative pathways of sesquiterpenoid hormones in arthropods (Hui et al 2010, 2013; Sin et al 2014; for details, refer to the main text); (C) summary of the presence of the sesquiterpenoid biosynthetic, degradative, and signaling pathway genes in the investigated arthropod genomes. “+” denotes presence and “−” represents the absence of supporting evidence.
Mentions: Sesquiterpenoids are a class of hydrocarbon/terpenes found in arthropods and plants; in arthropods, they are derived from the conversion of acetate via the mevalonate pathway (Tobe and Bendena 1999; Belles et al. 2005; Hui et al. 2010, 2013). In insects, there are two alternative pathways for the biosynthesis of JH: Either through the conversion of farnesoic acid (FA) to JH-III acid (JHA) by an epoxidase (CYP15C1) followed by methylation by JH acid methyltransferase (JHAMT) in the lepidopterans; or methylation of FA to MF by JHAMT followed by oxidation by another epoxidase (e.g., CYP15A1) as found in cockroaches and locust (Helvig et al. 2004; Belles et al. 2005; Marchal et al. 2011; Daimon et al. 2012; fig. 1A). In crustaceans, MF is synthesized through methylation of FA (Tobe et al. 1989). In addition to playing defensive roles in some social insects such as ants and bees, sesquiterpenoids including MF and JH are endogenously produced as master controllers of molting and sexual maturity in crustaceans and insects, respectively (Nagaraju 2007; Riddiford 2008). Although JH has never been identified in noninsect arthropods, JH mimics have been observed to play a role in controlling sex development and predator response in D. pulex (Olmstead and Leblanc 2002; Tatarazako et al. 2003; Miyakawa, Gotoh, et al. 2013). Recently, it has also been noted that the genes involved in JH production and degradation pathways, previously thought to be insect specific, are identified in water flea, shrimp, and centipede (Chipman et al. 2014; Sin et al. 2014). Here, we have identified JHAMT orthologs in the genomes of all investigated arthropods (fig. 1C and supplementary figs. S1 and S20, Supplementary Material online), suggesting the existence of a sesquiterpenoid biosynthetic system in the last common ancestor of all arthropods. However, no homologs of insect JH epoxidase (CYP15A1 or C1) could be identified in any of these noninsect arthropod genomes (fig. 1C). On the basis of this finding, we conclude, for the first time, that JH epoxidase was specifically gained in the insect lineage.Fig. 1.

Bottom Line: Moreover, we found that the "Broad-Complex" was specifically gained in the Pancrustacea, and the innovation of juvenile hormone (JH) in the insect linage correlates with the gain of the JH epoxidase (CYP15A1/C1) and the key residue changes in the binding domain of JH receptor ("Methoprene-tolerant").Furthermore, the gain of "Phantom" differentiates chelicerates from the other arthropods in using ponasterone A rather than 20-hydroxyecdysone as molting hormone.This study establishes a comprehensive framework for interpreting the evolution of these vital hormonal pathways in these most successful animals, the arthropods, for the first time.

View Article: PubMed Central - PubMed

Affiliation: Simon F.S. Li Marine Science Laboratory of School of Life Sciences and Center for Soybean Research of Partner State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong.

Show MeSH
Related in: MedlinePlus