Characterization of E93 in neometabolous thrips Frankliniella occidentalis and Haplothrips brevitubus

Abstract

Insect metamorphosis into an adult occurs after the juvenile hormone (JH) titer decreases at the end of the juvenile stage. This generally coincides with decreased transcript levels of JH-response transcription factors Krüppel homolog 1 (Kr-h1) and broad (br), and increased transcript levels of the adult specifier E93. Thrips (Thysanoptera) develop through inactive and non-feeding stages referred to as “propupa” and “pupa”, and this type of distinctive metamorphosis is called neometaboly. To understand the mechanisms of hormonal regulation in thrips metamorphosis, we previously analyzed the transcript levels of Kr-h1 and br in two thrips species, Frankliniella occidentalis (Thripidae) and Haplothrips brevitubus (Phlaeothripidae). In both species, the transcript levels of Kr-h1 and br decreased in the “propupal” and “pupal” stages, and their transcription was upregulated by exogenous JH mimic treatment. Here we analyzed the developmental profiles of E93 in these two thrips species. Quantitative RT-PCR revealed that E93 expression started to increase at the end of the larval stage in F. occidentalis and in the “propupal” stage of H. brevitubus, as Kr-h1 and br mRNA levels decreased. Treatment with an exogenous JH mimic at the onset of metamorphosis prevented pupal-adult transition and caused repression of E93. These results indicated that E93 is involved in adult differentiation after JH titer decreases at the end of the larval stage of thrips. By comparing the expression profiles of Kr-h1, br, and E93 among insect species, we propose that the “propupal” and “pupal” stages of thrips have some similarities with the holometabolous prepupal and pupal stages, respectively.

Knockdown of Ecdysone-Induced Protein 93F Causes Abnormal Pupae and Adults in the Eggplant Lady Beetle

“…Neometabolans undergo feeding larvae, non-feeding larvae with external wing primordial (propupal and pupal stages) and adults. Hemimetabolans move from immature nymphs to adults [ 1 , 2 , 3 ]. The identity of each stage and the transformation between them rely on two hormones, 20-hydroxyecdysone (20E) and juvenile hormones (JH) [ 4 , 5 , 6 , 7 , 8 ].…”

“…Secondly, the metamorphic transformation is involved in the presence of E93 [ 5 ] in some hemimetabolous [ 12 , 26 , 28 ], neometabolous [ 1 , 2 ] and holometabolous [ 13 , 29 , 30 ] insects. In the late stage of the last instar, the expression of Kr-h1 is declined.…”

“…Thirdly, E93 acts as an adult specifier [ 5 ]. Very high levels of E93 have been reported in the pupal stage in holometabolous insects and in the propupal and pupal stages in neometabolous Thysanopterans [ 2 , 9 , 13 ]. Knockdown of E93 in T. castaneum pupae inhibits adult transition and brings about an extra second pupae, clearly signifying that E93 serves as an adult specifier [ 26 ].…”

Transcriptome analysis of female western flower thrips, Frankliniella occidentalis, exhibiting neo-panoistic ovarian development

“…Except for Br expression in the embryonic stage, these two gene expression patterns followed the corresponding profiles of holometamorphic insects [ 33 ]. Furthermore, the adult specifier, E93 , expression increased during immature development and its inhibition prevented adult metamorphosis [ 34 ]. However, little is known about JH and ecdysteroid mediation in oogenesis in F .…”

“…JH acid methyltransferase (JHAMT), JH esterase/ JH epoxide hydrolase, and Met involved in JH synthesis, JH degradation, and the JH receptor, DEGs between transcripts at 0 h and 36 h after adult emergence and 60 h AAE represents DEGs between transcripts at 0 h and 60 h after adult emergence. KEGG categories include alanine, aspartate and glutamate metabolism (1), amino sugar and nucleotide sugar metabolism (2), apoptosis (3), arachidonic acid metabolism (4), ascorbate and aldarate metabolism (5), autophagy (6), biosynthesis of amino acids (7), biosynthesis of cofactors (8), biosynthesis of nucleotide sugars (9), biosynthesis of unsaturated fatty acids (10), carbon metabolism (11), citrate cycle (12), cysteine and methionine metabolism (13), cytochrome P450 ( 14), ECM-receptor interaction (15), endocytosis (16), fatty acid biosynthesis (17), fatty acid elongation (18), fatty acid metabolism (19),folate biosynthesis (20), foxO signaling pathway (21), fructose and mannose metabolism (22), glutathione metabolism (23), glycerolipid metabolism (24), glycerophospholipid metabolism (25), glycine, serine and threonine metabolism (26), glycolysis/gluconeogenesis (27), inositol phosphate metabolism (28), longevity regulating pathway (29), lysine degradation (30), lysosome (31), MAPK signaling pathway (32), metabolic pathways (33), mitophagy (34), glycan biosynthesis (35), nicotinate and nicotinamide metabolism (36), nucleotide metabolism (37), oxidative phosphorylation (38), pentose and glucoronate interconversions (39), pentose phosphate pathway (40), phagosome (41), protein export (42), protein processing in endoplasmic reticulum (43), purine metabolism (44), pyruvate metabolism (45), starch and sucrose metabolism (46), steroid biosynthesis (47), thiamine metabolism (48), Toll and Imd signaling pathway (49), various types of N-glycan biosynthesis (50), vitamin B6 metabolism (51), and Wnt signaling pathway (52).…”