Research Article: Transcriptome analysis of the molecular mechanism underlying immunity- and reproduction trade-off in Locusta migratoria infected by Micrococcus luteus

Date Published: August 14, 2019

Publisher: Public Library of Science

Author(s): Shaohua Wang, Xiaojun Liu, Zhiyong Xia, Guoqiang Xie, Bin Tang, Shigui Wang, Yulin Gao.


Immune response and reproductive success are two vital energy-consuming processes in living organisms. However, it is still unclear which process is prioritized when both are required. Therefore, the present study was designed to examine this question arising for one of the world’s most destructive agricultural pests, the migratory locust, Locusta migratoria. Transcripts from the ovaries and fat bodies of newly emerged locusts were analyzed, using RNA-seq based transcriptome and qualitative real-time PCR, at 4 h and 6 d after being infected with the gram-positive bacteria Micrococcus luteus. Changes in the main biological pathways involved in reproduction and immunization were analyzed using bioinformatics. After 4 h of infection, 348 and 133 transcripts were up- and down-regulated, respectively, whereas 5699 and 44 transcripts were up- and down-regulated, respectively, at 6 d after infection. Moreover, KEGG analysis indicated that vital pathways related with immunity and reproduction, such as Insulin resistance, FoxO signaling, Lysosome, mTOR signaling, and Toll-like receptor signaling pathways were up-regulated. Among the differentially expressed genes, 22 and 17 were related to immunity and reproduction, respectively. The expression levels of PPO1 and antimicrobial peptide defensin 3 were increased (log2FC = 5.93 and 6.75, respectively), whereas those of VgA and VgB were reduced (log2FC = -17.82 and -18.13, respectively). These results indicated that locust allocate energy and resources to maintain their own survival by increasing immune response when dealing with both immune and reproductive processes. The present study provides the first report of expression levels for genes related with reproduction and immunity in locusts, thereby providing a reference for future studies, as well as theoretical guidance for investigations of locust control.

Partial Text

Insects are one of the most successful group of animals on earth, owing, at least in part, to the effectiveness of their immune response to microbial invasion, which include both humoral and cellular immunity. Humoral immunity mainly deals with the synthesis of antimicrobial peptides (AMPs) in the fat body and is primarily based on the Toll and Imd signaling pathways, which play important roles in AMP expression, as well as on the interaction between the two pathways [1–2]. Meanwhile, cellular immunity involves hemocyte-mediated phagocytosis, encapsulation, and nodulation. The melanization of macroparasites triggered by hemocytes participating in phagocytosis or phenoloxidase cascade activation are hallmarks of cellular response [3]. Furthermore, the JNK and JAK/STAT pathways also contribute to the immune response [4]. During these immune processes, insects must invest energy and resources to survive against a variety of pathogens.

Resource trade-offs between immunity and reproduction may arise as a consequence of direct physiological conflicts between the two processes [10]. In the present study, the avirulent bacteria M. luteus was used to infect female L. migratoria, and the fat bodies and ovaries of the locusts were dissected at 4 h and 6 d after treatment. Female locusts develop to sexual maturity at ~5 d after eclosion, and energy and resource accumulate during this period. Significant changes in fat bodies and in ovaries start at 7 to 10 d after eclosion, and varieties of ingredients in fat bodies and ovaries increased rapidly since 10 d [15]. Bacterial infection often elicits long-term changes in global host transcription. For example, flies that have survived from M. luteus infection remain chronically infected with ~210 to 213 bacteria per fly for at least 5.5 d [16]. Considering that the early response includes both an aggressive initial immune response and injury-induced transcriptional regulation [17], infected insects were collected at 144 h (6 d) after treatment, with 4 h after treatment used as the control time point.

In this study, transcriptome analysis was used to identify M. luteus infection on the transcription of locust ovaries and fat bodies during the reproductive preparation period. The differentially expressed transcripts indicated that the expression of PPO1 and defensin 3 increased significantly, whereas the expression of Vgs decreased significantly, and that locusts, when faced with the trade-off of immune response and reproduction, allocate most resources to the physiological process of resistance to infection. These results provide a foundation for further studies of the molecular mechanisms underlying immune and reproductive trade-offs in locusts and provide insight for the biological control of locusts.




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