Labor division of worker ants can be controlled by insulin synthesis targeted through miR-279c-5p in Solenopsis invicta (Hymenoptera: Formicidae)

被引:5
作者
Chen, Jie [1 ]
Ma, Yunjie [1 ,2 ]
Guan, Ziying [1 ]
Liu, Qin [1 ]
Shi, Qingxing [1 ]
Qi, Guojun [1 ]
Chen, Ting [1 ]
Lyu, Lihua [1 ]
机构
[1] Guangdong Acad Agr Sci, Inst Plant Protect, Key Lab Green Prevent & Control Fruits & Vegetable, Guangdong Prov Key Lab High Technol Plant Protect,, Guangzhou 510640, Guangdong, Peoples R China
[2] South China Agr Univ, Coll Plant Protect, Dept Entomol, Guangzhou, Peoples R China
关键词
miR-279c-5p; labor division; Solenopsis invicta; social insects; ants; GENE-EXPRESSION; OF-LABOR; FIRE ANT; HONEY-BEES; SOCIAL REGULATION; BRAIN; PLASTICITY; MICRORNAS; EVOLUTION; BEHAVIOR;
D O I
10.1002/ps.7704
中图分类号
S3 [农学(农艺学)];
学科分类号
0901 ;
摘要
BACKGROUNDIn social insects, the labor division of workers is ubiquitous and controlled by genetic and environmental factors. However, how they modulate this coordinately remains poorly understood. RESULTSWe report miR-279c-5p participation in insulin synthesis and behavioral transition by negatively regulating Rab8A in Solenopsis invicta. Eusocial specific miR-279c-5p is age-associated and highly expressed in nurse workers, and localized in the cytoplasm of neurons, where it is partly co-localized with its target, Rab8A. We determined that miR-279c-5p agomir suppressed Rab8A expression in forager workers, consequently decreasing insulin content, resulting in the behavioral shift to 'nurse-like' behaviors, while the decrease in miR-279c-5p increased Rab8A expression and increased insulin content in nurse workers, leading to the behavioral shift to 'foraging-like' behaviors. Moreover, insulin could rescue the 'foraging behavior' induced by feeding miR-279c-5p to nurse workers. The overexpression and suppression of miR-279c-5p in vivo caused an obvious behavioral transition between foragers and nurses, and insulin synthesis was affected by miR-279c-5p by regulating the direct target Rab8A. CONCLUSIONWe first report that miR-279c-5p is a novel regulator that promotes labor division by negatively regulating the target gene Rab8A by controlling insulin production in ants. This miRNA-mediated mechanism is significant for understanding the behavioral plasticity of social insects between complex factors and potentially provides new targets for controlling red imported fire ants. & COPY; 2023 Society of Chemical Industry.
引用
收藏
页码:5029 / 5043
页数:15
相关论文
共 55 条
[31]  
Mott Christine M, 2012, Insects, V3, P1084, DOI 10.3390/insects3041084
[32]   Caste and sex specific olfactory glomerular organization and brain architecture in two sympatric ant species Camponotus sericeus and Camponotus compressus (Fabricius, 1798) [J].
Mysore, Keshava ;
Subramanian, K. A. ;
Sarasij, R. C. ;
Suresh, Arvind ;
Shyamala, Baragur V. ;
VijayRaghavan, K. ;
Rodrigues, Veronica .
ARTHROPOD STRUCTURE & DEVELOPMENT, 2009, 38 (06) :485-497
[33]   The gene vitellogenin has multiple coordinating effects on social organization [J].
Nelson, C. Mindy ;
Ihle, Kate E. ;
Fondrk, M. Kim ;
Page, Robert E., Jr. ;
Amdam, Gro V. .
PLOS BIOLOGY, 2007, 5 (03) :673-677
[34]   A methodology for the combined in situ analyses of the precursor and mature forms of microRNAs and correlation with their putative targets [J].
Nuovo, Gerard J. ;
Elton, Terry S. ;
Nana-Sinkam, Patrick ;
Volinia, Stefano ;
Croce, Carlo M. ;
Schmittgen, Thomas D. .
NATURE PROTOCOLS, 2009, 4 (01) :107-115
[35]   Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila [J].
Osborne, KA ;
Robichon, A ;
Burgess, E ;
Butland, S ;
Shaw, RA ;
Coulthard, A ;
Pereira, HS ;
Greenspan, RJ ;
Sokolowski, MB .
SCIENCE, 1997, 277 (5327) :834-836
[36]   The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.) [J].
Page, Robert E., Jr. ;
Scheiner, Ricarda ;
Erber, Joachim ;
Amdam, Gro V. .
CURRENT TOPICS IN DEVELOPMENTAL BIOLOGY, VOL 74, 2006, 74 :253-+
[37]   Thermoregulatory brood transport in the fire ant, Solenopsis invicta [J].
Penick, C. A. ;
Tschinkel, W. R. .
INSECTES SOCIAUX, 2008, 55 (02) :176-182
[38]   RNA editing is abundant and correlates with task performance in a social bumblebee [J].
Porath, Hagit T. ;
Hazan, Esther ;
Shpigler, Hagai ;
Cohen, Mira ;
Band, Mark ;
Ben-Shahar, Yehuda ;
Levanon, Erez Y. ;
Eisenberg, Eli ;
Bloch, Guy .
NATURE COMMUNICATIONS, 2019, 10 (1)
[39]   FIRE ANT POLYMORPHISM - THE ERGONOMICS OF BROOD PRODUCTION [J].
PORTER, SD ;
TSCHINKEL, WR .
BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 1985, 16 (04) :323-336
[40]   Characterization of Small RNAs in Aplysia Reveals a Role for miR-124 in Constraining Synaptic Plasticity through CREB [J].
Rajasethupathy, Priyamvada ;
Fiumara, Ferdinando ;
Sheridan, Robert ;
Betel, Doron ;
Puthanveettil, Sathyanarayanan V. ;
Russo, James J. ;
Sander, Chris ;
Tuschl, Thomas ;
Kandel, Eric .
NEURON, 2009, 63 (06) :803-817