Wolbachia-induced loss of male fertility is likely related to branch chain amino acid biosynthesis and iLvE in Laodelphax striatellus

• Published in: Insect biochemistry and molecular biology Vol. 85; pp. 11 - 20
• Main Authors: Ju, Jia-Fei, Hoffmann, Ary A., Zhang, Yan-Kai, Duan, Xing-Zhi, Guo, Yan, Gong, Jun-Tao, Zhu, Wen-Chao, Hong, Xiao-Yue
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.06.2017
• Subjects: Amino Acids - biosynthesis; Animals; BCAA biosynthesis; Copulation; Female; Fertility; Hemiptera - metabolism; Hemiptera - microbiology; Host-Pathogen Interactions; iLvE; Insect Proteins - metabolism; Laodelphax striatellus; Male; Male infertility; Oligonucleotide Array Sequence Analysis; Testis - metabolism; Transcriptome; Wolbachia; Wolbachia - physiology; Laodelphax striatellus; BCAA biosynthesis; iLvE; Wolbachia; Male infertility
• ISSN: 0965-1748; 1879-0240
• DOI: 10.1016/j.ibmb.2017.04.002

Wolbachia are endosymbionts that infect many species of arthropods and nematodes. Wolbachia-induced cytoplasmic incompatibility (CI) is the most common phenotype in affected hosts, involving embryonic lethality in crosses between Wolbachia-infected males and uninfected females. The molecular mechanisms underlying this phenomenon are currently unclear. Here we examine the molecular correlates of the Wolbachia infection in Laodelphax striatellus (Fallén), an important rice pest, where embryonic lethality is strong and almost complete. We compared the gene expression of 4-day-old Wolbachia-infected and uninfected L. striatellus testes to identify candidate genes for paternal-effect embryonic lethality induction. Based on microarray analysis, iLvE was the most down-regulated gene; this gene mediates branched-chain amino acid (BCAA) biosynthesis and participates in many processes related to reproductive performance. After knocking down iLvE by RNAi in uninfected male L. striatellus, male fertility was reduced, leading to a decrease in embryo hatching rates, but fertility was rescued in crosses between these males and Wolbachia-infected females. Removal of BCAA in chemically-defined diets of uninfected males also led to a loss of male fertility. Low amino acid nutrition may enhance exposure time of sperm to Wolbachia in the testes to affect adult reproduction in L. striatellus by reducing the number of sperm transferred per mating by males. These results indicate that Wolbachia may decrease male fertility in L. striatellus by acting on iLvE, a key factor of BCAA biosynthesis, and delaying sperm maturation. [Display omitted] •The aminotransferase iLvE might participate in Wolbachia-induced male infertility in the rice planthopper.•Knockdown of iLvE and a dietary reduction of BCAAs in Wolbachia-uninfected males mimics the male infertility phenotype.•Addition of dietary BCAAs partly rescues the male infertility phenotype in Wolbachia-infected males.•Wolbachia might slow sperm maturation through the BCAA biosynthesis pathway.