A First Glimpse of the Mexican Fruit Fly Anastrepha ludens (Diptera: Tephritidae) Antenna Morphology and Proteome in Response to a Proteinaceous Attractant
Abstract
:1. Introduction
2. Results
2.1. Morphological Features of Newly Emerged, Five- and 15-Day-Old Antennas
2.2. Proteome Profile of Antennas across Maturity Stages (Newly Emerged, Five-Day, and 15-Day Old Antennas)
2.3. Comparative Antenna Proteome Profile of A. ludens under Exposure of Ceratrap® by Tandem Mass Tags (TMT) and SPS-MS3 Approach
2.3.1. Odorant-Binding Proteins (OBPs)
2.3.2. Signal Transduction
2.3.3. Odorant Degrading Enzymes (ODEs)
3. Discussion
3.1. Flushing Out the Secrets of Olfactory Perception in A. ludens via the Characterization of the Antennal Proteome
3.2. CeraTrap® an Efficient Lure that Induces the Upregulation of the Olfactory Machinery of A. ludens
3.3. Integration of Proteomic Data to Help the Establishment of a New Generation of Tools for the Biorational Management of A. ludens
4. Materials and Methods
4.1. Chemical Reagents
4.2. Insect Rearing and Study Site
4.3. Light Microscopy (LM) Studies
4.4. Confocal Scanning Laser Microscopy (CSLM)
4.5. Scanning Electron Microscopy (SEM)
4.6. Anastrepha ludens Exposure to CeraTrap®
4.7. Protein Extraction
4.8. Trypsin Digestion, TMT Labeling, Simple Fractionation and Desalting
4.9. Fractionation of Labeled Peptide Mixture
4.10. Nano-LC-MS/MS Analysis
4.11. Decision Tree-Driven MS/MS
4.12. Synchronous Precursor Selection (SPS)-MS3 for TMT Analysis
4.13. Data Analyses and Interpretation
4.14. Real Time-Quantitative Polymerase Chain Reaction (RT-qPCR) Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
Ar | Arista |
AOX | Aldehyde oxidases |
BP | Biological processes |
Calr | Calreticulin |
Cam | Calmodulin |
CaMKII | Calcium/calmodulin-dependent protein kinase II |
COX | Cytochrome c oxidases |
Cpo | protein couch potato |
CSLM | Confocal scanning laser microscopy |
CSP | Chemosensory proteins |
Cyp DDT | Cytochromes P450 1-chloro-4-[2,2,2-trichloro-1-(4-chlorophenyl)ethyl]benzene |
EMR | Ezrin-moesin-radixin |
EST | Expressed sequence tag |
Flag | Flagellums |
GO | Gene ontology |
GRs | Gustatory receptors |
Gst | Glutathione S transferases |
IPM | Integrated pest management |
IRs | Ionotropic receptors |
iTRAQ | Isobaric tags for relative and absolute quantitation |
LM | Light microscopy |
ME | Methyl eugenol |
Ncc69 | Sodium chloride cotransporter 69 |
Nano-LC-MS/MS | Nanoscale liquid chromatography coupled to tandem mass spectrometry |
OBPs | Odorant-binding proteins |
ODE | Odorant-degrading enzymes |
ODPs | Odorant-degrading proteins |
ORs | Odorant receptors |
Orco | Odorant receptor co-receptor |
OSNs | Olfactory sensory neurons |
PBS | Phosphate buffered saline |
Ped | Pedicel |
Pka-R2 | cAMP-dependent, regulatory subunit type 2 |
PKC | Protein kinase C |
POBPA | Putative odorant-binding protein |
Pp2A-29B | Phosphatase 2A at 29B |
qRT-PCR | Quantitative real-time PCR |
Rtn | Reticulon-like protein |
RpS | Ubiquitin-40S ribosomal protein |
Sc | Scape |
SCX | Strong cation exchange |
SDS | Sodium dodecyl sulfate |
SDS-PAGE | Sodium dodecyl sulfate polyacrylamide gel electrophoresis |
SEM | Scanning electron microscopy |
SNMPs | Sensory neuron membrane proteins |
SPoCk | Secretory Pathway Calcium atpase |
(SPS)-MS | Synchronous precursor selection |
TMT | Tandem mass tags |
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Name. | Search Engine Score | |||
---|---|---|---|---|
Coverage | Mascot | Sequest | Amanda | |
Response to Pheromone (GO:0019236) | ||||
Odorant-binding protein 99b(Obp99b) | 20.3 | 41.6 | 8.9 | 1005.1 |
Odorant-binding protein 19a(Obp19a) | 5.4 | 60.4 | 2.2 | 329.1 |
Odorant-binding protein 99a(Obp99a) | 20.2 | 289.5 | 50.3 | 3044.6 |
Odorant-binding protein 28a(Obp28a) | 23.9 | 195.2 | 24.6 | 2393.9 |
General odorant-binding protein Lush (OBP Lush) | 18.9 | 58.2 | 10.5 | 1392.3 |
Odorant-binding protein 19d(Obp19d) | 8.8 | 261 | 22.4 | 873.6 |
Odorant-binding protein 99c, isoform B(Obp99c_B) | 11.6 | 128.1 | 10.9 | 1270.6 |
Odorant-binding protein 83a(Obp83a) | 42.9 | 460.1 | 59.4 | 2532.2 |
Odorant-binding protein 69a(Obp69a) | 23.9 | 218 | 28.1 | 500.4 |
Odorant-binding protein 44a(Obp44a) | 22.5 | 158.9 | 16.5 | 2334.1 |
Putative odorant-binding protein A10 | 51.6 | 586.3 | 87.2 | 7396 |
Sensory neuron membrane protein 1(Snmp1) | 12.1 | 68.3 | 9.7 | 1222.2 |
Odorant receptor co-receptor (Orco) | 13.5 | 58.2 | 7.9 | 948.7 |
Cellular Calcium Ion Homeostasis (GO:0006874) | ||||
Cation-transporting ATPase | 6.5 | 62.3 | 9.1 | 1085.3 |
Ryanodine receptor (RyR) | 1.1 | 94.8 | 8.8 | 800.4 |
upheld(up) | 32.2 | 564.1 | 105.7 | 10436 |
Plasma membrane calcium ATPase (PMCA) | 14.3 | 349.3 | 68 | 3815.5 |
Inositol 1,4,5,-tris-phosphate receptor(Itp-r83A) | 4.4 | 182.8 | 19.2 | 1969.8 |
Calreticulin (Calr) | 18.1 | 185.7 | 44.2 | 4205.3 |
Calnexin 99A(Cnx99A) | 25.2 | 269 | 49.2 | 5100.4 |
Calmodulin (Cam) | 79.1 | 513.6 | 73.1 | 5233.8 |
Calcium/calmodulin-dependent protein kinase II(CaMKII) | 18.8 | 193.5 | 22.4 | 2524 |
Secretory pathway calcium atpase (SPoCk) | 8.5 | 238.2 | 30.9 | 1887 |
Calmodulin-binding protein related to a Rab3 GDP/GTP exchange protein (Crag) | 2.9 | 56.6 | 3.2 | 551.3 |
Calcium-independent phospholipase A2 VIA (iPLA2-VIA) | 8.3 | 116.2 | 18.1 | 1589.9 |
Putative Odorant-Degrading Enzymes (ODE) | ||||
Cytochrome c oxidase subunit 5B(COX5B) | 10.8 | 56.3 | 5.4 | 471.5 |
Cytochrome c oxidase subunit 5A(COX5A) | 16 | 247 | 34 | 2052.4 |
Cytochrome c oxidase subunit 5A(COX5A) | 16 | 247 | 34 | 2052.4 |
Cytochrome c oxidase subunit 7A(COX7A) | 9.2 | 25 | 1.9 | 181.7 |
Glutathione S transferase E7(GstE7) | 26.1 | 241.4 | 39.3 | 3324.3 |
Juvenile hormone epoxide hydrolase 2(Jheh2) | 22.8 | 189.1 | 32.4 | 2632.6 |
Thioester-containing protein 4(Tep4) | 16 | 502.5 | 68.1 | 6495.8 |
Cytochrome P450-4d2(Cyp4d2) | 6.4 | 72.7 | 7.2 | 728.7 |
Cytochrome P450-9b2(Cyp9b2) | 15.5 | 170.6 | 35 | 3672.4 |
Cytochrome P450 reductase (Cpr) | 21.2 | 512.2 | 89 | 7761.4 |
Cytochrome P450-4e1(Cyp4e1) | 27.7 | 230.8 | 40.6 | 3214.5 |
Cytochrome P450-6a8(Cyp6a8) | 13.8 | 162.4 | 21.2 | 1942.7 |
Cytochrome P450 6a2 | 14.8 | 40.8 | 2.7 | 216.2 |
Probable cytochrome P450 6a23 | 7.6 | 119.3 | 11 | 1013.7 |
Glutathione S transferase S1(GstS1) | 22.5 | 179.7 | 32.6 | 3020.1 |
Glutathione S transferase E9(GstE9) | 19 | 281.4 | 30.7 | 3201.6 |
Glutathione S transferase D11(GstD11) | 30.6 | 300.9 | 36.5 | 3926.5 |
Glutathione S-transferase D1 | 38.1 | 740.2 | 136.1 | 8744.6 |
Microsomal glutathione S-transferase-like (Mgstl) | 8.4 | 54.22 | 3.3 | 398.9 |
Alpha-Est10 | 5.4 | 35.5 | 2.3 | 465.8 |
Thioester-containing protein 2(Tep2) | 3.2 | 48 | 10.4 | 912.2 |
Thioester-containing protein 2(Tep2) | 18.8 | 877.7 | 180 | 14738.1 |
Thioester-containing protein 3(Tep3) | 5.4 | 86.9 | 22.1 | 1787.1 |
Aldehyde dehydrogenase (Aldh) | 28.4 | 358.5 | 61.6 | 4366.4 |
Aldehyde oxidase 3(AOX3) | 11.4 | 705.6 | 112.3 | 11329.5 |
UDP-glycosyltransferase 35b(Ugt35b) | 5.8 | 25.5 | 1.9 | 325.1 |
Aldehyde oxidase 1 (AOX1) | 6.8 | 236.5 | 37.3 | 2716 |
Proteins | Code | 0D | 5D | 15D | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
2 h | 24 h | 2 h | 24 h | 2 h | 24 h | ||||||||
F | M | F | M | F | M | F | M | F | M | F | M | ||
Abundance Ratio:(CeraTrap®)/(Water) | |||||||||||||
Ubiquitin-40S ribosomal protein S27a (RpS27A) | P15357 | 2.0 | 1.4 | 2.1 | 1.7 | 2.4 | 2.1 | 0 | 1.2 | 0 | 1.1 | 2.2 | 1.2 |
Reticulon-like protein (Rtn1_c) | Q7KTP4 | 0 | 1.5 | 1.4 | 1.7 | 1.6 | 1.7 | 1.3 | 1.4 | 0 | 1.0 | 1.9 | 1.0 |
Sodium/potassium-transporting ATPase subunit alpha (Atpalpha) | P13607 | 0.9 | 1.7 | 1.7 | 1.7 | 1.5 | 1.7 | 1.5 | 1.5 | 0.3 | 1.0 | 1.9 | 1.1 |
PRL-1 phosphatase (PRL-1) | Q95VY8 | 0 | 0 | 1.6 | 1.7 | 1.3 | 1.6 | 1.3 | 1.5 | 0 | 0 | 0 | 1.3 |
Moesin/ezrin/radixin homolog 1, Ezrin-moesin-radixin 1 (EMR1) | P46150 | 1.8 | 1.4 | 1.6 | 1.6 | 1.5 | 1.7 | 1.4 | 1.4 | 0.6 | 1.3 | 2.1 | 1.1 |
Juvenile hormone-inducible protein 26 | Q7K0P0 | 0.7 | 0 | 1.4 | 1.6 | 1.3 | 1.4 | 1.5 | 1.3 | 0 | 1.4 | 0 | 1.1 |
Innexin inx2 (Inx2) | Q9V427 | 1.4 | 0 | 1.5 | 1.6 | 1.3 | 1.6 | 1.3 | 1.4 | 0 | 1.1 | 0 | 0 |
Voltage-dependent anion-selective channel (Porin) | Q94920 | 1.0 | 1.7 | 1.6 | 1.6 | 1.5 | 1.7 | 1.4 | 1.6 | 0.1 | 1.0 | 3.0 | 1.1 |
G protein alpha s subunit | P20354 | 0 | 0 | 1.6 | 1.6 | 1.1 | 1.5 | 1.4 | 1.4 | 0 | 1.1 | 0 | 1.6 |
plasma membrane calcium ATPase (PMCA) | Q59DP9 | 0.7 | 1.3 | 1.4 | 1.6 | 1.3 | 1.6 | 1.5 | 1.3 | 1.2 | 1.2 | 0 | 1.0 |
Secretory Pathway Calcium atpase (SPoCk) | Q9VNR2 | 0 | 0 | 1.5 | 1.6 | 1.1 | 1.7 | 1.3 | 1.4 | 0 | 1.3 | 0 | 0 |
Scribbled, isoform S (Scrib) | A0A0B4KHN3 | 0 | 0 | 1.1 | 1.6 | 1.8 | 1.7 | 1.3 | 1.2 | 0 | 0 | 0 | 1.1 |
Protein lap4 (LAP4) | Q7KRY7 | 0 | 1.3 | 1.7 | 1.6 | 1.0 | 1.4 | 1.3 | 1.4 | 0 | 1.3 | 2.3 | 1.3 |
Transient receptor potential cation channel protein painless (Pain) | Q9W0Y6 | 2.3 | 1.4 | 1.7 | 1.6 | 1.3 | 1.5 | 1.3 | 1.4 | 0 | 1.2 | 0 | 1.0 |
C-terminal Binding Protein | A4V2S3 | 0.7 | 0 | 1.4 | 1.6 | 1.2 | 1.4 | 1.5 | 1.3 | 0 | 1.1 | 2.7 | 1.3 |
NADPH:adrenodoxin oxidoreductase (Dare) | Q9V3T9 | 0 | 0 | 1.5 | 1.6 | 1.2 | 1.4 | 1.4 | 1.3 | 0 | 1.1 | 0 | 1.1 |
Calreticulin (Calr) | P29413 | 1.8 | 1.3 | 1.7 | 1.6 | 1.4 | 1.5 | 1.5 | 1.2 | 0.6 | 1.4 | 0.8 | 1.1 |
Protein phosphatase 2A at 29B (Pp2A-29B) | P36179 | 0 | 1.5 | 1.5 | 1.6 | 1.0 | 1.5 | 1.1 | 1.2 | 0 | 1.1 | 0 | 1.4 |
Sodium chloride cotransporter 69 (Ncc69) | Q9VTW8 | 0.8 | 0 | 1.6 | 1.5 | 1.4 | 1.7 | 1.3 | 1.4 | 0 | 1.1 | 0 | 1.2 |
Reticulon-like protein (Rtn1) | Q9VMV9 | 1.8 | 1.5 | 1.5 | 1.5 | 1.5 | 1.4 | 1.4 | 1.3 | 0.3 | 1.1 | 0 | 1.0 |
Reticulon-like protein (Rtn1_b) | E1JHT6 | 0 | 0 | 1.5 | 1.5 | 1.5 | 1.4 | 1.4 | 1.3 | 0.1 | 1.1 | 0 | 1.0 |
Receptor of activated protein kinase C 1n (PKC) | M9PCC1 | 0.7 | 1.5 | 1.5 | 1.5 | 1.4 | 1.7 | 1.4 | 1.6 | 0 | 1.4 | 0 | 1.0 |
Protein couch potato (Cpo) | Q01617 | 0 | 0 | 1.6 | 1.5 | 1.4 | 1.5 | 1.3 | 1.4 | 0 | 1.5 | 0 | 1.0 |
Protein kinase, cAMP-dependent, catalytic subunit 1 | P12370 | 0 | 0 | 0 | 1.5 | 1.2 | 1.4 | 1.3 | 1.4 | 0 | 1.0 | 0 | 1.2 |
Protein kinase, cAMP-dependent, regulatory subunit type 2 | P81900 | 0 | 1.6 | 1.6 | 1.5 | 1.4 | 1.5 | 1.3 | 0 | 0 | 1.1 | 0 | 1.7 |
G protein beta-subunit 13F | P26308 | 0 | 1.2 | 1.3 | 1.5 | 1.4 | 1.7 | 1.3 | 0 | 0 | 1.2 | 0 | 1.0 |
Calcium/calmodulin-dependent protein kinase type II (CaMKII) | Q00168 | 0 | 0 | 1.6 | 1.5 | 1.2 | 1.5 | 1.5 | 1.4 | 0 | 1.1 | 0 | 0 |
Sensory neuron membrane protein 1 (Snmp1) | Q9VDD3 | 1.6 | 1.4 | 1.8 | 1.5 | 1.1 | 1.5 | 1.4 | 1.5 | 0.9 | 1.3 | 0 | 1.0 |
Calmodulin | P62152 | 1.0 | 1.5 | 1.5 | 1.4 | 1.2 | 1.5 | 1.4 | 1.2 | 0 | 1.6 | 0 | 1.1 |
AMP deaminase (AMPdeam) | Q9VY76 | 0 | 0 | 1.4 | 1.4 | 1.3 | 1.6 | 1.4 | 1.4 | 0.4 | 1.0 | 0 | 0 |
Adenylate kinase 3 | Q9VGU6 | 0 | 0 | 1.3 | 1.4 | 1.2 | 1.3 | 1.2 | 1.3 | 0 | 1.0 | 0 | 1.1 |
UDP-glucose 6-dehydrogenase | O02373 | 0 | 0 | 1.8 | 0 | 0 | 0 | 0 | 0 | 0 | 1.0 | 0 | 0 |
Aquaporin | Q9V5Z7 | 0 | 0 | 1.7 | 0 | 1.1 | 0 | 1.3 | 1.4 | 0.1 | 1.0 | 0 | 0 |
Receptor-type guanylate cyclase | Q7JQ32 | 0 | 0 | 0 | 0 | 1.3 | 0 | 0 | 0 | 0.1 | 0 | 0 | 0 |
Odorant receptor co-receptor (Orco) | Q9VNB5 | 0.6 | 0 | 1.5 | 1.5 | 1.2 | 1.4 | 1.3 | 1.6 | 0 | 1.4 | 0 | 0 |
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Ruiz-May, E.; Altúzar-Molina, A.; Elizalde-Contreras, J.M.; Arellano-de los Santos, J.; Monribot-Villanueva, J.; Guillén, L.; Vázquez-Rosas-Landa, M.; Ibarra-Laclette, E.; Ramírez-Vázquez, M.; Ortega, R.; et al. A First Glimpse of the Mexican Fruit Fly Anastrepha ludens (Diptera: Tephritidae) Antenna Morphology and Proteome in Response to a Proteinaceous Attractant. Int. J. Mol. Sci. 2020, 21, 8086. https://doi.org/10.3390/ijms21218086
Ruiz-May E, Altúzar-Molina A, Elizalde-Contreras JM, Arellano-de los Santos J, Monribot-Villanueva J, Guillén L, Vázquez-Rosas-Landa M, Ibarra-Laclette E, Ramírez-Vázquez M, Ortega R, et al. A First Glimpse of the Mexican Fruit Fly Anastrepha ludens (Diptera: Tephritidae) Antenna Morphology and Proteome in Response to a Proteinaceous Attractant. International Journal of Molecular Sciences. 2020; 21(21):8086. https://doi.org/10.3390/ijms21218086
Chicago/Turabian StyleRuiz-May, Eliel, Alma Altúzar-Molina, José M. Elizalde-Contreras, Jiovanny Arellano-de los Santos, Juan Monribot-Villanueva, Larissa Guillén, Mirna Vázquez-Rosas-Landa, Enrique Ibarra-Laclette, Mónica Ramírez-Vázquez, Rafael Ortega, and et al. 2020. "A First Glimpse of the Mexican Fruit Fly Anastrepha ludens (Diptera: Tephritidae) Antenna Morphology and Proteome in Response to a Proteinaceous Attractant" International Journal of Molecular Sciences 21, no. 21: 8086. https://doi.org/10.3390/ijms21218086