Cytosolic and mitochondrial ribosomal proteins mediate the locust phase transition via divergence of translational profiles
Saturday, 2023/02/04 | 07:18:26
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Jing Li, Liya Wei, Yongsheng Wang, Haikang Zhang, Pengcheng Yang, Zhangwu Zhao and Le Kang.
PNAS January 26, 2023; 120 (5) e2216851120 https://doi.org/10.1073/pnas.2216851120 SignificanceOutbreaks of locust plagues are largely attributed to the phase transition from solitary to gregarious locusts. Many studies have demonstrated transcriptional and posttranslational regulation in phase change. However, the translational regulation in the locust phase transition is unclear. Here, we found plasticity in polysome profiles between solitary and gregarious locusts. A divergence with ribosomal proteins from cytoplasm and mitochondria modulates behavioral features of gregarious and solitary locusts. The findings reveal that the population density of locusts, as an environmental signal, can initiate translational regulation for the phenotypic plasticity of insects. Important clues in searching for targets to control pests are also provided. Insights into energy metabolism regulation at the translational level in eukaryotes are presented as well. AbstractThe phase transition from solitary to gregarious locusts is crucial in outbreaks of locust plague, which threaten agricultural yield and food security. Research on the regulatory mechanisms of phase transition in locusts has focused primarily on the transcriptional or posttranslational level. However, the translational regulation of phase transition is unexplored. Here, we show a phase-dependent pattern at the translation level, which exhibits different polysome profiles between gregarious and solitary locusts. The gregarious locusts exhibit significant increases in 60S and polyribosomes, while solitary locusts possess higher peaks of the monoribosome and a specific “halfmer.” The polysome profiles, a molecular phenotype, respond to changes in population density. In gregarious locusts, ten genes involved in the cytosolic ribosome pathway exhibited increased translational efficiency (TE). In solitary locusts, five genes from the mitochondrial ribosome pathway displayed increased TE. The high expression of large ribosomal protein 7 at the translational level promotes accumulation of the free 60S ribosomal subunit in gregarious locusts, while solitary locusts employ mitochondrial small ribosomal protein 18c to induce the assembly of mitochondrial ribosomes, causing divergence of the translational profiles and behavioral transition. This study reveals the translational regulatory mechanism of locust phase transition, in which the locusts employ divergent ribosome pathways to cope with changes in population density.
See https://www.pnas.org/doi/10.1073/pnas.2216851120
Figure 1: Polysome profile differences between gregarious and solitary locusts. (A) Absorbance (A254 nm) of sucrose density gradient-fractionated ribosomes from RNase I- or mock-treated (control) gregarious locusts. (B) Absorbance (A254 nm) of sucrose density gradient fractionated ribosomes from RNase I- or mock-treated (control) solitary locusts. (C) Mass spectrometry (MS/MS) analysis of proteins in fractions 5, 7, and 9 of the sucrose density gradient. (D) Absorbance (A254 nm) of sucrose density gradient fractions measured from ribosomes in gregarious locusts. (E) Absorbance (A254 nm) of sucrose density gradient fractions measured from ribosomes in solitary locusts. (F) Different polysome profiles from gregarious and solitary locusts. The X-axis indicates thetop (fraction 1) to the bottom (fraction 15) from 0 mm to 75 mm of the 5 to 50% sucrose gradient. The Y-axis indicates the absorbance (A254 nm) from ribosomes. The red arrowheads indicate specific peaks in solitary locusts. Yellow regions highlight 60S ribosomal subunits and polyribosomes. (G) Quantification of polysome peak sizes of gregarious and solitary locusts in representative experiments with n = 3, normalized to the P1 peak of solitary locusts. The normalized method was performed as in a previous study (30). Bars represent the mean ± SEM, and significance was tested with Student’s t test, with *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001. (H) The number of differential abundance proteins from 60S fractions in gregarious and solitary locusts was detected by mass spectrometry (MS/MS). The 60S fractions contain the 60S large ribosomal subunit and 60S mitochondrial ribosomes in locusts. The higher abundance of proteins (MS/MS count fold change > 1.2) in gregarious locusts than solitary locusts was defined as Up in G, while the higher abundance of proteins (MS/MS count fold change > 1.2) in solitary locusts than gregarious locusts was defined as Up in S. |
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