Morphology, sex steroid level and gene expression analysis in gonadal sex reversal of triploid female (XXX) rainbow trout (Oncorhynchus mykiss)

Abstract

In non-mammalian vertebrates, estrogens and expressions of cyp19a1 and foxl2 play critical roles in maintaining ovary differentiation and development, while dmrt1 and sox9 are male-specific genes in testicular differentiation and are highly conserved. In order to deeply understand the morphological change, sex steroids level and molecular mechanism of triploid female gonadal reversal in rainbow trout, we studied the ovary morphology, tendency of estradiol-17β (E2) and testosterone (T) levels and the relative expressions of dmrt1, cyp19a1, sox9 and foxl2 in juvenile and adult fish. Our results demonstrated that the development of triploid female gonads in rainbow trout went through arrested development, oocytes dedifferentiation, ovary reconstruction and sex reversal finally. During early gonadal development (154-334 days post-fertilization), the expressions of foxl2 and cyp19a1 increased linearly, while expressions of dmrt1 and sox9 were extremely suppressed, and E2 level was higher, while T level was lower. During the mid-to-late period of triploid female gonadal development (574-964 days post-fertilization), the expressions of dmrt1 and sox9 remained high and were very close to the quantity of diploid male genes, and T levels were even reaching diploid male plasma concentrations, while expressions of cyp19a1 and foxl2 were decreased, leading to decrease in E2 level. We realized that the development model of rainbow trout triploid female gonads was extremely rare, and the regulatory mechanism was very special. Genes involved in gonadal development and endogenous estrogens are pivotal factors in fish natural sex reversal.

Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster

“…Within the Salmoninae, differentiated gonochorism where primordial germ cells develop directly into testis or ovarian tissues has been described in, for example, Arctic charr ( Salvelinus alpinus ) 4 , brook charr ( Salvelinus fontinalis ) 55 , brown trout ( Salmo trutta ) 56 , rainbow trout ( O . mykiss ) 57 , and coho salmon ( O . kisutch) 58 .…”

Comprehensive analysis of miRNA-mRNA/lncRNA during gonadal development of triploid female rainbow trout (Oncorhynchus mykiss)

“…According to a previous study, rainbow trout showed the presence of undifferentiated gonads before 67 dpf, the gonad was composed mainly of primordial germ cells (PGCs) at this period (Feist & Schreck, 1996). The gonadal development of triploid rainbow begins to show abnormal characteristics after 154 dpf, and the gonadal morphology was very different between diploid and triploid after 574 dpf (Xu et al, 2016). The histological analysis of gonadal morphology of 180 dpf and 600 dpf were shown in Fig.…”

Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster

“…Within the Salmoninae, differentiated gonochorism where primordial germ cells develop directly into testis or ovarian tissues has been described in, for example, Arctic charr ( Salvelinus alpinus ) 4 , brook charr ( Salvelinus fontinalis ) 50 , brown trout ( Salmo trutta ) 51 , rainbow trout ( O. mykiss ) 52 , and coho salmon ( O. kisutch) 53 . The European grayling as representative of the Thymallinae instead shows a rare form of undifferentiated gonochorism, since undifferentiated gonochoristic species usually go through an all-female stage before they differentiate into testis and ovaries 1 .…”