Comparative analysis of locomotor behavior and head diurnal transcriptome regulation by PERIOD and CRY2 in the diamondback moth

Feb 28, 2024Insect science

Differences in daily movement and gene activity controlled by PERIOD and CRY2 proteins in the diamondback moth

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Abstract

1,098 genes exhibited rhythmic expression in wild-type diamondback moths.

Rhythmic expressions of the Pxper and Pxcry2 genes were observed in the heads of P. xylostella, with differing phases.
PxCRY2 was found to repress transcriptional activation of CLOCK:BMAL1 in vitro, while PxPER did not have a similar effect.
Knocking out either Pxper or Pxcry2 eliminated the activity peak after lights-off in light-dark cycles.
Loss of Pxcry2 reduced overall activity and was essential for maintaining endogenous rhythms in constant darkness.
749 of the 1,098 rhythmic genes in wild-type P. xylostella relied on Pxper and Pxcry2 for their rhythmic expression.
Most core clock genes lost their rhythmicity in mutants lacking Pxper and Pxcry2, while Pxcry2 maintained rhythmic expression but with altered characteristics.

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Earth's rotation shapes a 24-h cycle, governing circadian rhythms in organisms. In mammals, the core clock genes, CLOCK and BMAL1, are regulated by PERIODs (PERs) and CRYPTOCHROMEs (CRYs), but their roles remain unclear in the diamondback moth, Plutella xylostella. To explore this, we studied P. xylostella, which possesses a simplified circadian system compared to mammals. In P. xylostella, we observed rhythmic expressions of the Pxper and Pxcry2 genes in their heads, with differing phases. In vitro experiments revealed that PxCRY2 repressed monarch butterfly CLK:BMAL1 transcriptional activation, while PxPER and other CRY-like proteins did not. However, PxPER showed an inhibitory effect on PxCLK/PxCYCLE. Using CRISPR/Cas9, we individually and in combination knocked out Pxper and Pxcry2, then conducted gene function studies and circadian transcriptome sequencing. Loss of either Pxper or Pxcry2 eliminated the activity peak after lights-off in light-dark cycles, and Pxcry2 loss reduced overall activity. Pxcry2 was crucial for maintaining endogenous rhythms in constant darkness. Under light-dark conditions, 1 098 genes exhibited rhythmic expression in wild-type P. xylostella heads, with 749 relying on Pxper and Pxcry2 for their rhythms. Most core clock genes lost their rhythmicity in Pxper and Pxcry2 mutants, while Pxcry2 sustained rhythmic expression, albeit with reduced amplitude and altered phase. Additionally, rhythmic genes were linked to biological processes like the spliceosome and Toll signaling pathway, with these rhythms depending on Pxper or Pxcry2 function. In summary, our study unveils differences in circadian rhythm regulation by Pxper and Pxcry2 in P. xylostella. This provides a valuable model for understanding circadian clock regulation in nocturnal animals.

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Comparative analysis of locomotor behavior and head diurnal transcriptome regulation by PERIOD and CRY2 in the diamondback moth

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