Effects of heat stress on follicular development and atresia in Nile tilapia (Oreochromis niloticus) during one reproductive cycle and its potential regulation by autophagy and apoptosis

Abstract

Nile tilapia (Oreochromis niloticus) ovulates and releases eggs many times a year, and its suitable spawning temperature is 22 °C–28 °C. High temperature limits its success in reproduction. The purpose of this study was to explore the effects of heat stress (34.5 °C ± 0.5) on follicular development and atresia in female Nile tilapia. We analyzed tissue sections, serum hormone contents, gene transcript levels, fatty acid composition, and the transcriptome of the ovary of Nile tilapia. Compared with the control group, the heat-stressed group showed significantly reduced gonadal weight and gonadosomatic index of female fish. Morphological analyses revealed that heat stress increased follicular atresia and induced apoptosis and autophagy in the ovary. Heat stress also led to decreased serum contents of luteinizing hormone, follicle-stimulating hormone, and estradiol, and decreased transcript levels of genes encoding their corresponding receptors (LHR, FSHR, and ER). The transcript levels of genes related to apoptosis (Bcl2, Bim, caspase-3) and autophagy (Bax, Beclin-1, LC3a) increased in response to heat stress, accompanied by increased follicular atresia. Fish in the heat-stressed group showed decreased contents of fat, monounsaturated fatty acids, and polyunsaturated fatty acids, but increased saturated fatty acid content, in the ovary, indicative of dysfunctional fat synthesis and utilization. Differentially expressed mRNAs under heat stress were mainly involved in apoptosis and autophagy, metabolism, and hormone regulation signaling. Specifically, p53-, NOD-like receptor-, and MAPK-signaling pathways associated with apoptosis and autophagy were dysregulated under heat stress. Together, these results suggest that the combination of apoptosis and autophagy modulate follicular atresia of Nile tilapia under heat stress.