A β-carotene-binding protein carrying a red pigment regulates body-color transition between green and black in locusts

Meiling Yang,Qing Liu,Xiaojiao Guo,Yanli Wang,Zhikang Liu,Jianzhen Zhang,Le Kang,Feng Jiang,Huimin Wang

doi:10.7554/elife.41362

Abstract

Changes of body color have important effects for animals in adapting to variable environments. The migratory locust exhibits body color polyphenism between solitary and gregarious individuals, with the former displaying a uniform green coloration and the latter having a prominent pattern of black dorsal and brown ventral surface. However, the molecular mechanism underlying the density-dependent body color changes of conspecific locusts remain largely unknown. Here, we found that upregulation of β-carotene-binding protein promotes the accumulation of red pigment, which added to the green color palette present in solitary locusts changes it from green to black, and that downregulation of this protein led to the reverse, changing the color of gregarious locusts from black to green. Our results provide insight that color changes of locusts are dependent on variation in the red β-carotene pigment binding to βCBP. This finding of animal coloration corresponds with trichromatic theory of color vision.

Highlights

Body color change is a ubiquitous but highly diverse phenomenon of adaptive significance to animals under exposure to illnesses, environmental changes, predation, and sexual signals (Burmeister et al, 2005; Henderson et al, 2017; Mathger et al, 2003; Stuart-Fox and Moussalli, 2008; Teyssier et al, 2015)
We identified a total of 1653 differentially expressed genes (DEGs) between the gregarious and solitary locusts (Figure 1—figure supplement 1A), and 26% (430) of these DEGs were protein-coding genes (Figure 1—figure supplement 1B)
Consistent with the deeper black color of the pronotum than of the tergum of the thorax and abdomen in gregarious locusts, we found that b-carotene-binding protein (bCBP) expression was significantly higher in the pronotum than in the tergum integuments of the thorax and abdomen in gregarious locusts, whereas little bCBP expression was observed in the terga of solitary locusts, with no variability among the tergum segments (Figure 2A)

Summary

Introduction

Body color change is a ubiquitous but highly diverse phenomenon of adaptive significance to animals under exposure to illnesses, environmental changes, predation, and sexual signals (Burmeister et al, 2005; Henderson et al, 2017; Mathger et al, 2003; Stuart-Fox and Moussalli, 2008; Teyssier et al, 2015). Rapid and reversible color change is a rare trait regulated by endogenous and exogenous mechanisms (Cuthill et al, 2017; Hubbard et al, 2010). This type of phenotypic plasticity has not been well investigated. Rapid body color changes in arthropods such as aphids, locusts and grasshoppers, lepidopteran caterpillars, and spider mites are influenced by environmental changes, especially by changes in population density (Bryon et al, 2017; Tabadkani et al, 2013; Valverde and Schielzeth, 2015; Wang and Kang, 2014; Xiong et al, 2017). Similar to that of other animals (Cuthill et al, 2017; Duarte et al, 2017), the coloration of locusts serves as a dynamic form of population information

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Conclusion