Temperature Significantly Regulates Gene Expressions of Vertebrae Chondrocytes and Osteoblasts in Juvenile Golden Pompano (Trachinotus ovatus)

Mingyang Han,Rui Yang,Jian G Qin,Zhengyi Fu,Zhenhua Ma

doi:10.3389/fmars.2021.668522

Abstract

To elucidate the possible molecular reaction of vertebral fusion in juvenile golden pompano at high temperature, we examined the changes in growth, vertebral fusion incidence, histological differences and transcription levels of genes related to bone development in juvenile golden pompano at 27 and 33°C for 30 days, respectively. The growth rate of juvenile fish was faster when the water temperature was 33°C, but the incidence of vertebral fusion was higher. Prolonged high water temperature reduced the osteogenic layer in the growth zone of the vertebral endplate and the elastic externa. The endplate growth areas of the fused vertebrae were transformed into cartilage tissue, which was then remodeled into bone. The intervertebral notochord tissue was transformed into bone and the intervertebral space disappeared. In normal phenotypes of vertebrae, short-term high temperature could promote the expression of genes related to cartilage differentiation and maturation, as well as genes related to osteoblastic differentiation. With the increase of culture time, the expression of genes related to cartilage and osteogenesis development was inhibited. In fused vertebrae, cartilage proliferation was enhanced, osteogenic differentiation was inhibited, and matrix mineralization may be enhanced. Genes associated with the development of chondrocytes and osteoblasts in the vertebrae of juvenileTrachinotus ovatuswere significantly regulated by temperature and time. The results may contribute to further understanding of the occurrence of vertebral fusion at high temperature.

Highlights

The vertebral column, composed of vertebrae and joint tissues, is an important fundamental infrastructure unique to vertebrates (Fleming et al, 2015; Galbusera and Bassani, 2019) and could provide structural support and protection for the organism (Scaal, 2016)
The results of this study showed that high water temperature could accelerate the growth of juvenile golden pompano, but it led to the increase of vertebral fusion over time
The homeostasis of the intervertebral tissue was altered by long-term high temperature (HT) cultivation

Summary

Introduction

The vertebral column, composed of vertebrae and joint tissues, is an important fundamental infrastructure unique to vertebrates (Fleming et al, 2015; Galbusera and Bassani, 2019) and could provide structural support and protection for the organism (Scaal, 2016). The abnormalities of the vertebral column are frequently observed in farmed fish, which is one of the important factors restricting the development of the aquaculture industry (Pedersen et al, 2011). Vertebral fusion is a common type of spinal abnormality. In farmed Atlantic salmon (Salmo salar), for example, fusion is the most common type of spinal deformity (Witten et al, 2009; Fjelldal et al, 2012). Existing research suggests that transformation, remodeling, and replacement of intervertebral tissue eventually lead to vertebral fusion, which involves alterations in extracellular matrix (ECM) components, metaplastic chondrogenesis and mineralization (Witten et al, 2006; Pedersen et al, 2011; Davie et al, 2019). The occurrence of vertebral fusion is externally regulated by rearing temperature and nutritional factors (Ytteborg et al, 2010a; Wu et al, 2016; Munday et al, 2018)

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