Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts

  1. Dafeng Chen
  2. Li Hou
  3. Jianing Wei
  4. Siyuan Guo
  5. Weichan Cui
  6. Pengcheng Yang
  7. Le Kang  Is a corresponding author
  8. Xianhui Wang  Is a corresponding author
  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, China
  2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, China
  3. Beijing Institutes of Life Sciences, Chinese Academy of Sciences, China
5 figures and 3 additional files

Figures

Figure 1 with 2 supplements
Olfactory signals from gregarious male adults trigger the synchrony of female sexual maturation in locusts.

(A) Distribution of the first oviposition time of gregarious and solitarious phases. The first oviposition date was recorded after 6 days post adult eclosion (PAE 6 days) when individuals began to …

Figure 1—source data 1

Raw data for first oviposition time and sexual maturity of gregarious, solitarious, and Orco-/- female adults.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig1-data1-v1.xlsx
Figure 1—figure supplement 1
Comparison of sexual maturation rate of gregarious and solitarious females.

The maturity of terminal oocytes in gregarious and solitarious females were measured from post adult eclosion (PAE) 2 to 8 days. Data were analyzed using Student’s t-test. The number of biological …

Figure 1—figure supplement 1—source data 1

Raw data for maturation rate of females between gregarious and solitarious phases.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig1-figsupp1-data1-v1.xlsx
Figure 1—figure supplement 2
Schematic diagram of the stimulation experiments for females of the migratory locust.

(A) Ten gregarious females were reared with 10 gregarious males or 10 gregarious females after emergence, respectively. (B) One solitarious female was reared with one solitarious male or one …

Figure 2 with 3 supplements
4-Vinylanisole abundantly released by gregarious male adults promotes sexual maturation synchrony of female locusts.

(A) Dynamic changes in volatiles released from gregarious male adults, gregarious female adults, and solitarious male adults from post adult eclosion (PAE) 1 to 8 days. (B) The maturity of …

Figure 2—source data 1

Raw data for volatile contents in adults and sexual maturity of females.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
Releasing dynamics of 14 identified volatiles in gregarious male adults, gregarious female adults, and solitarious male adults from post adult eclosion (PAE) 1 to 8 days.

Gregarious male adults release much more phenylacetonitrile (PAN), guaicol, 4-vinylanisole, vertrole, and anisole than gregarious female adults and solitarious male adults after PAE 4 days. Data are …

Figure 2—figure supplement 2
Dose-dependent effects of 4-vinylanisole (4-VA) on female maturation rate.

Different letters represent significant differences between the two groups (one-way ANOVA, p < 0.05). The number of biological replicates was shown in the figures.

Figure 2—figure supplement 2—source data 1

Raw data for maturation rate of females treated by 4-vinylanisole (4-VA).

https://cdn.elifesciences.org/articles/74581/elife-74581-fig2-figsupp2-data1-v1.xlsx
Figure 2—figure supplement 3
The sexual maturity of wild-type (WT) females and Or35-/- females after stimulation by volatiles released from gregarious males (n = 20, Levene’s test, p = 0.02; Student’s t-test, ***p < 0.001).

Lines in droplet diagram indicate median quartile.

Figure 2—figure supplement 3—source data 1

Raw data for sexual maturity of wild-type (WT) females and Or35-/- females stimulated by volatiles released from gregarious males.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig2-figsupp3-data1-v1.xlsx
Figure 3 with 6 supplements
4-Vinylanisole (4-VA) promotes sexual maturation synchrony in young females by enhancing juvenile hormone/vitellogenin (JH/Vg) signaling pathway at post adult eclosion (PAE) 3–4 days.

(A) The 4-VA effects on sexual maturity of gregarious virgin females at different developmental stages. (B) Dosage effects on electroantennography (EAG) responses of females to 4-VA at different …

Figure 3—source data 1

Raw data for sexual maturity, juvenile hormone (JH) titer, gene expression, and protein level in 4-vinylanisole (4-VA)-treated females.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig3-data1-v1.xlsx
Figure 3—figure supplement 1
Effects of gregarious males with different ages on maturation synchrony of female aged at post adult eclosion (PAE) 3–4 days.

Gregarious females aged at PAE 3 days were reared together with the fifth-instar gregarious males, or male adults aged at PAE 1 day, PAE 3 days, PAE 5 days for 2 days, respectively. Data were …

Figure 3—figure supplement 1—source data 1

Raw data for sexual maturity of females reared with gregarious males with different ages.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig3-figsupp1-data1-v1.xlsx
Figure 3—figure supplement 2
Enrichment of differentially expressed genes (DEGs) and Kyoto encyclopedia of genes and genomes (KEGG) in the fat body of gregarious females after 4-vinylanisole (4-VA) stimulation at different developmental stages.

Gene expression pattern showed the most dynamic changes in the fat body of females exposed to 4-VA at post adult eclosion (PAE) 3–4 days.

Figure 3—figure supplement 3
Peripheral electrophysiological responses of female locusts to 4-vinylanisole (4-VA).

(A) and (B) Dosage effects on single sensilla responses (SSRs) of basiconic sensillum in females to 4-VA. (C) The SSR of basiconic sensillum in females to 4-VA aged at different developmental …

Figure 3—figure supplement 3—source data 1

Raw data for electrophysiological responses of female locusts to 4-vinylanisole (4-VA).

https://cdn.elifesciences.org/articles/74581/elife-74581-fig3-figsupp3-data1-v1.xlsx
Figure 3—figure supplement 4
The mRNA levels of LmigOr35 during post adult eclosion (PAE) 1–8 days.

Different letters represent significant differences (one-way ANOVA, p < 0.05). Points labeled with different letters indicate a significant difference between these groups. Data are shown as means ± …

Figure 3—figure supplement 4—source data 1

Raw data for mRNA levels of LmigOr35 during post adult eclosion (PAE) 1–8 days.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig3-figsupp4-data1-v1.xlsx
Figure 3—figure supplement 5
Volcano plot of RNA-seq data in the brain of females treated by 4-vinylanisole (4-VA) at post adult eclosion (PAE) 3–4 days.

There were 52 downregulated and 37 upregulated genes in the brain of female locusts upon 4-VA treatment, respectively.

Figure 3—figure supplement 6
The mRNA level of JHAMT and JHE upon 4-vinylanisole (4-VA) treatment.

Student’s t-test, n = 4, *p < 0.05, **p < 0.01. Data are shown as means ± SEM.

Figure 3—figure supplement 6—source data 1

Raw data for mRNA level of JHAMT and JHE upon 4-vinylanisole (4-VA) treatment.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig3-figsupp6-data1-v1.xlsx
Figure 4 with 1 supplement
Juvenile hormone/vitellogenin (JH/Vg) pathway indeed mediates the stimulatory effects of 4-vinylanisole (4-VA) on female sexual maturation.

(A) JH titers in the hemolymph of wild-type (WT) and Or35-/- females after stimulation by 4-VA at post adult eclosion (PAE) 3–4 days. (B) The mRNA levels of Vg in the fat body and (C) protein levels …

Figure 4—source data 1

Raw data for juvenile hormone (JH) titer, gene expression, protein level, and sexual maturity in wild-type (WT) and Or35-/- females.

https://cdn.elifesciences.org/articles/74581/elife-74581-fig4-data1-v1.xlsx
Figure 4—figure supplement 1
Validation the role of Or35 in 4-vinylanisole (4-VA)-enhanced vitellogenin (Vg) expression in the fat body of female locusts.

(A) The protein levels of Vg in the fat body of wild-type (WT) females and Or35-/- females with or without 4-VA treatment. Student’s t-test: n = 4, *p < 0.05, n.s. indicates not significant. Data …

Figure 4—figure supplement 1—source data 1

Raw data for vitellogenin (Vg) expression in the fat body of female locusts stimulated by 4-vinylanisole (4-VA).

https://cdn.elifesciences.org/articles/74581/elife-74581-fig4-figsupp1-data1-v1.xlsx
Schematic mechanisms underlying 4-vinylanisole (4-VA)-induced synchrony of female sexual maturation.

4-VA released from gregarious male locusts can significantly accelerate the ovary development of females with less-developed ovaries (approximately before post adult eclosion [PAE] 4 days) but not …

Additional files

Supplementary file 1

List of genes related to juvenile hormone (JH) synthesis and degradation in the corpus cardiacum-corpora allatum (CC-CA) of female adults exposure to 4-vinylanisole (4-VA) at post adult eclosion (PAE) 3–4 days.

https://cdn.elifesciences.org/articles/74581/elife-74581-supp1-v1.xlsx
Supplementary file 2

Primers used in qPCR analysis.

https://cdn.elifesciences.org/articles/74581/elife-74581-supp2-v1.docx
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