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
[1]   Meta-analysis of genome-wide expression patterns associated with behavioral maturation in honey bees [J].
Adams, Heather A. ;
Southey, Bruce R. ;
Robinson, Gene E. ;
Rodriguez-Zas, Sandra L. .
BMC GENOMICS, 2008, 9 (1)
[2]   MicroRNA miR-7 Regulates Secretion of Insulin-Like Peptides [J].
Agbu, Pamela ;
Cassidy, Justin J. ;
Braverman, Jonathan ;
Jacobson, Alec ;
Carthew, Richard W. .
ENDOCRINOLOGY, 2020, 161 (02)
[3]   Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies [J].
Ament, Seth A. ;
Corona, Miguel ;
Pollock, Henry S. ;
Robinson, Gene E. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (11) :4226-4231
[4]   MicroRNAs in Honey Bee Caste Determination [J].
Ashby, Regan ;
Foret, Sylvain ;
Searle, Iain ;
Maleszka, Ryszard .
SCIENTIFIC REPORTS, 2016, 6
[5]   Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee [J].
Behura, S. K. ;
Whitfield, C. W. .
INSECT MOLECULAR BIOLOGY, 2010, 19 (04) :431-439
[6]   Influence of gene action across different time scales on behavior [J].
Ben-Shahar, Y ;
Robichon, A ;
Sokolowski, MB ;
Robinson, GE .
SCIENCE, 2002, 296 (5568) :741-744
[7]   Compositional heterogeneity and outgroup choice influence the internal phylogeny of the ants [J].
Borowiec, Marek L. ;
Rabeling, Christian ;
Brady, Sean G. ;
Fisher, Brian L. ;
Schultz, Ted R. ;
Ward, Philip S. .
MOLECULAR PHYLOGENETICS AND EVOLUTION, 2019, 134 :111-121
[8]   A functional study of miR-124 in the developing neural tube [J].
Cao, Xinwei ;
Pfaff, Samuel L. ;
Gage, Fred H. .
GENES & DEVELOPMENT, 2007, 21 (05) :531-536
[9]   Task selection by workers of the fire ant Solenopsis invicta [J].
Cassill, DL ;
Tschinkel, WR .
BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY, 1999, 45 (3-4) :301-310
[10]   Social regulation of insulin signaling and the evolution of eusociality in ants [J].
Chandra, Vikram ;
Fetter-Pruneda, Ingrid ;
Oxley, Peter R. ;
Ritger, Amelia L. ;
McKenzie, Sean K. ;
Libbrecht, Romain ;
Kronauer, Daniel J. C. .
SCIENCE, 2018, 361 (6400) :398-+