Genome-wide profiling of piRNAs in the whitefly, Bemisia tabaci reveals cluster distribution and potential association with begomovirus transmission

Authors: Shamimuzzaman, Md - Shamim; Hasegawa, Daniel; CHEN, WENBO - Boyce Thompson Institute; Simmons, Alvin; FEI, ZHANGJUN - Boyce Thompson Institute; Ling, Kai-Shu

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/5/2019
Publication Date: 3/12/2019
Citation: Shamimuzzaman, M., Hasegawa, D.K., Chen, W., Simmons, A.M., Fei, Z., Ling, K. 2019. Genome-wide profiling of piRNAs in the whitefly, Bemisia tabaci reveals cluster distribution and potential association with begomovirus transmission. PLoS One. 14(3):e0213149. https://doi.org/10.1371/Journal.pone.0213149.
DOI: https://doi.org/10.1371/Journal.pone.0213149

Interpretive Summary: Small RNAs are 19-31 nucleotide (nt) non-coding regulatory elements commonly found in plants, animals and insects. They play an important role in regulation of gene expression, transposable elements (TE) and parasite immunity. Major classes of small RNAs include small interfering RNAs (siRNAs) and microRNAs (miRNAs), which are primarily involved in silencing gene expression. In addition to the above two classes, another class of small RNAs known as PIWI-interacting RNAs (piRNAs) has been identified in vertebrate and invertebrate animals. piRNAs regulate the activity of transposable elements as well as silence the expression of protein coding genes. In this study, in collaboration with Boyce Thompson Institute, ARS scientists, for the first time, conducted genome-wide profiling of piRNAs in the whitefly, Bemisia tabaci that could also be involved in association with begomovirus transmission. Knowledge of the mechanisms on how the piRNA pathway regulates reproduction and antiviral immune responses in whitefly could be useful for both fundamental and applied research. Our enhanced understanding of piRNA pathway in whitefly will facilitate the identification of novel targets for whitefly control using RNA interference and genome editing technologies.

Technical Abstract: Piwi-interacting RNAs (piRNAs) are 26-31 nucleotide (nt) non-coding small RNAs (sRNAs) commonly found in animals. The whitefly, Bemisia tabaci MEAM1 is a notorious vector capable of transmitting many plant viruses, resulting in serious crop loss and food shortage around the world. To investigate potential sRNA-mediated regulatory mechanisms in whiteflies that are affected by virus acquisition and transmission, we conducted sRNA deep sequencing and performed genome-wide profiling of piRNAs in whiteflies that fed on tomato yellow leaf curl virus (TYLCV)-infected plants or non-infected tomato control plants for 24, 48, and 72 h. The number of piRNAs ranged from 564,395 to 1,715,652 per treatment and time point, and aggregated in 57 to 96 clusters in the whitefly genome. Comparative analysis identified 53 expressed piRNA clusters that were expressed in all treatments. We also identified five TYLCV-induced and 24 TYLCV-suppressed piRNA clusters. Approximately 62% of all identified piRNAs were derived from non-coding sequences that include intergenic regions, introns, and UTRs with unknown functions. The remaining 38% of piRNAs were derived from coding sequences (CDS) and repeat elements. Six protein coding genes including COMM domain-containing protein, sentrin-specific protease, and mitochondrial carrier protein were targeted by the TYLCV-induced piRNAs. Transposable elements targeted by piRNA clusters include both class I retrotransposons such as Gypsy, Copia, and LINEs and class II DNA transposons such as MITE, hAT, and TcMar. Characterization and understanding of whitefly piRNAs and their target genes or regulatory elements might facilitate the identification of novel genetic targets for whitefly management.