Transcriptome of Tetranychus urticae embryos reveals insights into Wolbachia‐induced cytoplasmic incompatibility

Abstract

The endosymbiont Wolbachia is known for manipulating host reproduction in selfish ways. However, the molecular mechanisms have not yet been investigated in embryos. Here, we found that Wolbachia had no effect on the number of deposited eggs in Tetranychus urticae Koch (Acari: Tetranychidae) but caused two types of reproductive manipulation: killing uninfected female embryos via cytoplasmic incompatibility (CI) and increasing the hatching ratio of infected female embryos. RNA sequencing analyses showed that 145 genes were differentially expressed between Wolbachia‐infected (WI) and Wolbachia‐uninfected (WU) embryos. Wolbachia infection down‐regulated messenger RNA (mRNA) expression of glutathione S‐transferase that could buffer oxidative stress. In addition, 1613 and 294 genes were identified as CI‐specific up‐/down‐regulated genes. Compared to WU and WI embryos, embryos of CI cross strongly expressed genes involved in transcription, translation, tissue morphogenesis, DNA damage and mRNA surveillance. In contrast, most of the genes associated with energy production and metabolism were down‐regulated in the CI embryos compared to the WU and WI embryos, which provides some clues as to the cause of death of CI embryos. These results identify several genes that could be candidates for explaining Wolbachia‐induced CI. Our data form a basis to help elucidate the molecular consequences of CI in embryos.

The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria

“…Several reports, however, provide clues about what host pathways might be affected by or mediate Wolbachia-induced CI. As noted earlier, analysis of the transcriptional changes in spider mite embryos resulting from incompatible crosses has highlighted the up-regulation of DNA-damage response and chromatin-related genes, among other targets [73].…”

“…The delays in histone deposition on paternal DNA, paternal nuclear envelope breakdown, and activation of the mitotic kinase Cdk1, as well as abnormal paternal chromosome condensation and segregation have all been speculated to be downstream effects related to a fundamental DNA defect in the paternal chromosome set [13,14,29,33]. In the previously mentioned transcriptome analysis of T. urticae embryos from CI crosses, the DNA damage response was among the upregulated gene pathways [73].…”

“…However, these findings are intriguing because of their connection to the earliest known defects observed in embryos from incompatible crosses (see above), which is the delay in maternal histone incorporation into the chromatin of the male pronucleus [29]. In a recent study of the transcriptome of Tetranychus urticae (spider mite) embryos, genes involved in histone modifications and the histone genes themselves were among the genes whose expression significantly changed in Wolbachia-mediated CI crosses compared to wild-type or rescue crosses [73]. CidB may cause defects in histone deposition by altering the ubiquitylation of histones or histone chaperones involved in nucleosome formation.…”

Symbiont-Mediated Cytoplasmic Incompatibility: What have we Learned in 50 Years?

“…of CI surmises that both CifA and CifB must be expressed in males to cause CI, and CifA must be expressed in females to rescue CI . (B) CifA and CifB coevolve and are classified into at least five different phylogenetic Types (1-5) (Bing et al, 2019;LePage et al, 2017;Lindsey et al, 2018).…”

“…Since then, the availability of additional genomes and Cif sequences have exposed at least five clades referred to as Types 1-5 ( Fig. 3B) (Bing et al, 2019;Lindsey et al, 2018), and highly divergent Cif-like homologs in Orientia and Rickettsia bacteria (Gillespie et al, 2018). It is likely that continued genomic sequencing will reveal additional Cif phylogenetic Types.…”