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Int J Mol Sci
2022 May 26;2311:. doi: 10.3390/ijms23115998.
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Rethinking Sesquiterpenoids: A Widespread Hormone in Animals.
So WL, Kai Z, Qu Z, Bendena WG, Hui JHL.
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The sesquiterpenoid hormone juvenile hormone (JH) controls development, reproduction, and metamorphosis in insects, and has long been thought to be confined to the Insecta. While it remains true that juvenile hormone is specifically synthesized in insects, other types or forms of sesquiterpenoids have also been discovered in distantly related animals, such as the jellyfish. Here, we combine the latest literature and annotate the sesquiterpenoid biosynthetic pathway genes in different animal genomes. We hypothesize that the sesquiterpenoid hormonal system is an ancestral system established in an animal ancestor and remains widespread in many animals. Different animal lineages have adapted different enzymatic routes from a common pathway, with cnidarians producing farnesoic acid (FA); non-insect protostomes and non-vertebrate deuterostomes such as cephalochordate and echinoderm synthesizing FA and methyl farnesoate (MF); and insects producing FA, MF, and JH. Our hypothesis revolutionizes the current view on the sesquiterpenoids in the metazoans, and forms a foundation for a re-investigation of the roles of this important and yet neglected type of hormone in different animals.
Figure 1. JH signaling pathway.Schematic diagram showing the cellular response upon JH stimulation, summarized from the previous literature. JH binds to its intracellular receptor Methoprene-tolerant (Met) and the complex is transported into the nucleus, mediated by heat shock protein 83 (Hsp83). Steroid receptor coactivator (SRC) then forms a heterodimer with the JH-Met to form an active complex to regulate the transcription of target genes. A putative transmembrane receptor (labeled in pale green with a dotted line) is hypothesized from previous studies, which demonstrated an activated intracellular RTK-signaling pathway (phospholipase C (PLC), phosphatidylinositol biphosphatein (PIP2), diacylglycerol (DAG), inositol trisphosphate (IP3), and Ca2+/calmodulin-dependent protein kinase II (CaMKII)) in JH-stimulating cells.
Figure 2. A summary of the literature reporting the gene cassette required in sesquiterpenoid biosynthesis and the JHAMT gene tree. (A) A table showing the presence of MVA, isoprenylation and JH-specific pathway in different animals, summarized from the previous studies [21,23,46,49,50,51,52,58]. The box labeled in green with “+” indicates the presence of genes; The box labeled in red with “-” indicates the absence of genes. The box labeled in grey with “?” indicates the uncertainty. The genes present in the mevalonate pathway, the isoprenylation pathway, and the downstream juvenile hormone pathway are highlighted in orange, green, and blue, respectively. ACAT, Acetyl-CoA Acetyltransferase; HMGCS, hydroxymethylglutaryl-CoA synthase; HMGCR, 3-hydroxy-3-methylglutaryl-CoA reductase; MVK, mevalonate kinase; PMVK, phosphomevalonate kinase; DPMD, diphosphomevalonate decarboxylase; FPPS, farnesyl diphosphate synthase; FPPP, farnesyl diphosphate phosphatase; FOHSDR, farnesol dehydrogenase (short-chain dehydrogenase); ALDHIII, aldehyde dehydrogenase 3; PFT, protein farnesyl transferase; STE24, endopeptidase; ICMT, protein-S-isoprenylcysteine O-methyltransferase; PCYOX, prenylcysteine oxidase. (B) Phylogenetic gene tree of JHAMTs identified in animals. The tree topology shown is constructed by the maximum likelihood (ML) algorithm. The phylogenetic trees were constructed with the LG + G + I model using the maximum likelihood (ML) and neighbor-joining (NJ) methods, rooted with arthropod farnesoic methyltransferase (FAMeT) in MEGA 7.0, with 1000 replicates. Only bootstrap values larger than 80% are indicated for clarity (blue from ML and red from NJ).
Figure 3. The form of sesquiterpenoids present across the animal phylogeny and their biological effects documented in previous studies.
Figure 4. A summary of the sesquiterpenoid biosynthetic pathway and the putative functioning final products in different researched animals up to date. The enzymes in the mevalonate pathway, the isoprenylation pathway, and the downstream JH-specific pathway are highlighted in orange, green, and blue, respectively.
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