The reproductive systems of female insects have been the subject of extensive study, primarily because of their potential as targets for insect control. Adequate accumulation of vitellin (Vn) in the oocyte is essential for insect ovary development and embryo maturation (Tufail and Takeda 2008). The accumulation of Vn involves the production of large amounts of vitellogenin (Vg) and the uptake of Vg by oocytes (Pszczolkowski et al., 2005). The production of large amounts of vitellogenin requires insects to store sufficient nutrients, and the permeability of the follicular epithelium is key to allowing Vg to reach the oocyte plasma membrane (Huebner and Injeyan, 1981, Heier et al., 2021, Arrese and Soulages, 2010). In addition, both the interstitial matrix and the basement membrane undergo continuous remodelling during normal oogenesis and egg maturation (Haigo and Bilder, 2011, Pearson et al., 2016a, Pearson et al., 2016b). A previous study revealed that changes in the follicular cell program are involved in the reorganization of the cytoskeleton or associated with the basement membrane, which is a specialized class of extracellular matrix (ECM) proteins (Pearson et al., 2016a, Pearson et al., 2016b). The ECM consists of a fibrous network of glycoproteins and proteoglycans (Hynes and Naba, 2012). The ovarian ECM is rich in collagen, laminin and fibrin, and in addition to providing structural support, the ECM is essential for regulating stem cell fate, organ morphogenesis and signaling (Hynes, 2009, Tang, 2020). Studies have shown that ECM remodeling leads to follicle growth and oocyte release during ovulation (Pearson et al., 2016a, Pearson et al., 2016b, Díaz-Torres et al., 2021). Thus, extracellular matrix metabolism and tissue homeostasis are tightly coordinated during oogenesis.

Secreted Protein, Acidic and Rich in Cysteine, (SPARC, also known as BM40 and osteonectin) is a multifunctional calcium-binding cell-matrix glycoprotein (Sage et al., 1984, Martinek et al., 2002, Koehler et al., 2009). As a functionally conserved collagen-binding protein, SPARC plays an important role in regulating interactions between cells and their surrounding ECM, as well as controlling fundamental cellular functions such as cell adhesion, proliferation and differentiation (Wong and Sukkar, 2017). It appears to be conserved from invertebrates to vertebrates and is involved in diverse functions. SPARC has been shown to be required for early morphological development in Xenopus, and its absence results in many tissue defects after hatching (Purcell Pszczolkowski et al., 1993). Moreover, adequate levels of SPARC are essential for normal development and muscle function in Caenorhabditis elegans (Schwarzbauer and Spencer, 1993). The effect of SPARC has been studied in Drosophila melanogaster. Its multiple functions in embryonic development, heart formation and egg chamber elongation have been revealed (Martinek et al., 2008, Volk et al., 2014, Isabella and Horne-Badovinac, 2015). A previous study showed that SPARC is involved in maintaining mitosis and the cytoskeletal arrangement of follicular cells in Blattella germanica (Irles Pszczolkowski et al., 2017). In addition, SPARC plays a role in glucose and energy homeostasis during development. The absence of SPARC exacerbates high-fat diet-induced diabetes in mice, and SPARC-deficient mice develop systemic metabolic disorders (Aoi et al., 2019, Atorrasagasti et al., 2019). Studies have shown that SPARC-deficient mice have reduced glucose tolerance and impaired insulin secretion (Hu Pszczolkowski et al., 2020). Mouse SPARC regulates heat production in adipocytes and induces lipolysis and fat oxidation (Aoi Pszczolkowski et al., 2019). Deletion of SPARC disrupts fat body homeostasis in Drosophila melanogaster larvae (Shahab Pszczolkowski et al., 2015). In the rice brown planthopper (Nilaparvata lugens Stal), disruption of SPARC resulted in a significant reduction in the number of eggs and offspring, as well as reduction in fat body content (Wang Pszczolkowski et al., 2022). SPARC has been studied in only a limited number of invertebrate species. However, the role of SPARC in locusts is unclear.

L. migratoria has a high reproductive rate and causes great damage to organic agriculture (Peng Pszczolkowski et al., 2020). In this study, we used RNA interference (RNAi) technology to investigate the effect of the LmSPARC gene on locust ovarian development. Combined with the results of transcriptomic and metabolomic analyses, we also revealed that LmSPARC plays a role in the process of lipid metabolism. This study identified a new target for the control of this global pest using RNAi technology, as well as providing a reference for the molecular mechanism by how LmSPARC influences locust ovarian development.