Transcriptome profiling reveals that differences in regulatory patterns of gonad development between male and female largemouth bass (Micropterus salmoides) contribute to dimorphic weight gain

Abstract

Background Largemouth bass (Micropterus salmoides) is a sexually dimorphic oviparous species with a significant disparity in gonad size between males and females. Analyzing the mechanism of gonad development is crucial for studying individual growth and development in largemouth bass. Methods In this study, histological analyses, transcriptome sequencing, and fluorescent in situ hybridization analyses were employed to examine the disparities in gonad development between male and female largemouth bass. Results The results indicated a significantly higher growth rate of females than of males, with the ovaries exhibiting greater fullness than the testes. The weight of the mature ovaries was four to five times that of the testes. High transcript levels of acsl5, cidec, lrp13, and elovl1a in the ovary were related to the accumulation of lipid droplets and yolk particles in oocytes. Among the genes with high transcript levels in the ovary, gdf9, ccnb1, ldlrap1a, srd5a1, hsd17b12a, and lfng encoded proteins involved in the regulation of follicle development, oocyte proliferation and differentiation, and steroid hormone synthesis to promote ovarian development. Some of the genes showing high transcript levels in the testes (tekt1, mns1, lrguk, spag6, spef2, and nme5) were implicated in flagella formation, and tdrd5 and star were involved in sperm development. Some of the identified sex-determining genes also exerted significant influences on gonad development. The gene dmrt1, which was specific expressed in spermatogonia, likely plays a crucial role in cell proliferation, whereas btg4, which was specific expressed in the cytoplasm of female oocytes, may participate in regulating meiosis and facilitating oocyte cytoplasm maturation. Conclusions There was an enhancement in the biosynthesis of lipid droplets and yolk granules in oocytes, increasing oocytes cell growth and proliferation. As well as a significant number of genes concentrated on the formation of sperm flagella and other structures. Differences in gene expression led to an increase in the difference in volume between spermatogonia and oocytes during their respective maturation processes, resulting in a significant disparity in both size and weight between the testes and the ovaries. Our findings offer valuable insights into the mechanisms underlying gonad development of largemouth bass.