Limits...
Transciptomic and histological analysis of hepatopancreas, muscle and gill tissues of oriental river prawn (Macrobrachium nipponense) in response to chronic hypoxia.

Sun S, Xuan F, Fu H, Zhu J, Ge X, Gu Z - BMC Genomics (2015)

Bottom Line: Oriental river prawn, Macrobrachium nipponense, is a commercially important species found in brackish and fresh waters throughout China.However, the effects of dissolved oxygen availability on gene expression and physiological functions of those tissues of prawns are unknown.Genes from well known functional categories and signaling pathways associated with stress responses and adaptation to extreme environments were significantly enriched, including genes in the functional categories "response to stimulus", "transferase activity" and "oxidoreductase activity", and the signaling pathways "oxidative phosphorylation", "glycolysis/gluconeogenesis" and "MAPK signaling".

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Genetic Breeding and Aquaculture Biology of Freshwater Fishes, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, People's Republic of China. sunshengming621416@163.com.

ABSTRACT

Background: Oriental river prawn, Macrobrachium nipponense, is a commercially important species found in brackish and fresh waters throughout China. Chronic hypoxia is a major physiological challenge for prawns in culture, and the hepatopancreas, muscle and gill tissues play important roles in adaptive processes. However, the effects of dissolved oxygen availability on gene expression and physiological functions of those tissues of prawns are unknown. Adaptation to hypoxia is a complex process, to help us understand stress-sensing mechanism and ultimately permit selection for hypoxia- tolerant prawns, we performed transcriptomic analysis of juvenile M. nipponense hepatopancreas, gill and muscle tissues by RNA-Seq.

Results: Approximately 46,472,741; 52,773,612 and 58,195,908 raw sequence reads were generated from hepatopancreas, muscle and gill tissues, respectively. A total of 62,722 unigenes were generated, of the assembled unigenes, we identified 8,892 genes that were significantly up-regulated, while 5,760 genes were significantly down-regulated in response to chronic hypoxia. Genes from well known functional categories and signaling pathways associated with stress responses and adaptation to extreme environments were significantly enriched, including genes in the functional categories "response to stimulus", "transferase activity" and "oxidoreductase activity", and the signaling pathways "oxidative phosphorylation", "glycolysis/gluconeogenesis" and "MAPK signaling". The expression patterns of 18 DEGs involved in hypoxic regulation of M. nipponense were validated by quantitative real-time reverse-transcriptase polymerase chain reactions (qRT-PCR; average correlation coefficient = 0.94). In addition, the hepatopancreas and gills exhibited histological differences between hypoxia and normoxia groups. These structural alterations could affect the vital physiological functions of prawns in response to chronic hypoxia, which could adversely affect growth and survival of M. nipponense.

Conclusions: Gene expression changes in tissues from the oriental river prawn provide a preliminary basis to better understand the molecular responses of M. nipponense to chronic hypoxia. The differentially expressed genes (DEGs) identified in M. nipponense under hypoxia stress may be important for future genetic improvement of cultivated prawns or other crustaceans through transgenic approaches aimed at increasing hypoxia tolerance.

No MeSH data available.


Related in: MedlinePlus

Histopathological changes in the hepatopancreas, gill and muscle. Hepatopancreas of the Macrobrachium nipponense following a 7-day exposure to hypoxia: (a) control prawns; (b) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen, showing the appearance of large numbers of vacuoles in the tubular epithelial cells and abnormal lumens. ALU, abnormal lumen; MEL, melanization of cells; REC, ruptured epithelial cells. Anterior gill lamellae of the M. nipponense following a 7-day exposure to hypoxia: (c) control prawns showing normal lamellae structure and intact pillar cells (PC); (d) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing disrupted pillar cells (PC*), necrosis (NCR) and extensive infiltration of haemocytes (HAE). Histological cross sections of muscle of (e) control group and (f) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing simialr striated muscle fibers infiltrated by hemocytes (small arrowhead). Scale bars = 50 μm
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4490754&req=5

Fig6: Histopathological changes in the hepatopancreas, gill and muscle. Hepatopancreas of the Macrobrachium nipponense following a 7-day exposure to hypoxia: (a) control prawns; (b) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen, showing the appearance of large numbers of vacuoles in the tubular epithelial cells and abnormal lumens. ALU, abnormal lumen; MEL, melanization of cells; REC, ruptured epithelial cells. Anterior gill lamellae of the M. nipponense following a 7-day exposure to hypoxia: (c) control prawns showing normal lamellae structure and intact pillar cells (PC); (d) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing disrupted pillar cells (PC*), necrosis (NCR) and extensive infiltration of haemocytes (HAE). Histological cross sections of muscle of (e) control group and (f) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing simialr striated muscle fibers infiltrated by hemocytes (small arrowhead). Scale bars = 50 μm

Mentions: The hepatopancreas is composed of numerous blind-end tubules, with each tubule consisting of different epithelial cell types, i.e. E-cell (embryonic), R-cell (resorptive), F-cell (fibrillar) and B-cell (blisterlike) [71]. Histological analysis of the hepatopancreas has been used as a practical means for assessing the environmental stress in the shrimp culture [72–74]. The R-cells in hepatopancreas epithelia are known to function as the main site for lipid storage [74]. There were distinct differences in the condition of the hepatopancreas in M. nipponense from normoxia and hypoxia groups (Fig. 6a & b). The most obvious abnormalities were the hypertrophy of B-cells, and vacuoles that tended to coalesce into larger ones. Also, the number of B-cells was increased under hypoxia. The R-cells were compressed, appeared cuboidal and were reduced in number. The tubule lumens were mis-shaped and were enlarged due to a thinned epithelium. In crustaceans, the hepatopancreas is used for monitoring culture health and it serves as a sensitive indicator for metabolism, nutritional status and diseases in various shrimp species because it is the site of digestion, nutrient absorption, reserve storage, and synthesis and secretion of digestive enzymes [75, 76]. Our study has also captured indirect evidence that oxidative stress suppressed antioxidant gene expression and disrupted fatty acid metabolism due to the observation of vacuolation in R-cells. The histoarchitecture of gills in the hypoxia group showed hemocytic infiltration, fused gill lamellae, mild malformations, swollen and necrotic lamellae, and complete disorganization of lamellae (Fig. 6c & d). All these incidents can eventually lead to gill injury, which leads to disturbance in oxygen consumption [77] and enzymatic activities [78] in aquatic organisms. However, no obvious alterations were observed by light microscopy in the muscle tissues of M. nipponense after chronic hypoxia (Fig. 6e & f).Fig. 6


Transciptomic and histological analysis of hepatopancreas, muscle and gill tissues of oriental river prawn (Macrobrachium nipponense) in response to chronic hypoxia.

Sun S, Xuan F, Fu H, Zhu J, Ge X, Gu Z - BMC Genomics (2015)

Histopathological changes in the hepatopancreas, gill and muscle. Hepatopancreas of the Macrobrachium nipponense following a 7-day exposure to hypoxia: (a) control prawns; (b) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen, showing the appearance of large numbers of vacuoles in the tubular epithelial cells and abnormal lumens. ALU, abnormal lumen; MEL, melanization of cells; REC, ruptured epithelial cells. Anterior gill lamellae of the M. nipponense following a 7-day exposure to hypoxia: (c) control prawns showing normal lamellae structure and intact pillar cells (PC); (d) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing disrupted pillar cells (PC*), necrosis (NCR) and extensive infiltration of haemocytes (HAE). Histological cross sections of muscle of (e) control group and (f) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing simialr striated muscle fibers infiltrated by hemocytes (small arrowhead). Scale bars = 50 μm
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4490754&req=5

Fig6: Histopathological changes in the hepatopancreas, gill and muscle. Hepatopancreas of the Macrobrachium nipponense following a 7-day exposure to hypoxia: (a) control prawns; (b) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen, showing the appearance of large numbers of vacuoles in the tubular epithelial cells and abnormal lumens. ALU, abnormal lumen; MEL, melanization of cells; REC, ruptured epithelial cells. Anterior gill lamellae of the M. nipponense following a 7-day exposure to hypoxia: (c) control prawns showing normal lamellae structure and intact pillar cells (PC); (d) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing disrupted pillar cells (PC*), necrosis (NCR) and extensive infiltration of haemocytes (HAE). Histological cross sections of muscle of (e) control group and (f) prawns exposed to hypoxia at 2.5 mg/L dissolved oxygen showing simialr striated muscle fibers infiltrated by hemocytes (small arrowhead). Scale bars = 50 μm
Mentions: The hepatopancreas is composed of numerous blind-end tubules, with each tubule consisting of different epithelial cell types, i.e. E-cell (embryonic), R-cell (resorptive), F-cell (fibrillar) and B-cell (blisterlike) [71]. Histological analysis of the hepatopancreas has been used as a practical means for assessing the environmental stress in the shrimp culture [72–74]. The R-cells in hepatopancreas epithelia are known to function as the main site for lipid storage [74]. There were distinct differences in the condition of the hepatopancreas in M. nipponense from normoxia and hypoxia groups (Fig. 6a & b). The most obvious abnormalities were the hypertrophy of B-cells, and vacuoles that tended to coalesce into larger ones. Also, the number of B-cells was increased under hypoxia. The R-cells were compressed, appeared cuboidal and were reduced in number. The tubule lumens were mis-shaped and were enlarged due to a thinned epithelium. In crustaceans, the hepatopancreas is used for monitoring culture health and it serves as a sensitive indicator for metabolism, nutritional status and diseases in various shrimp species because it is the site of digestion, nutrient absorption, reserve storage, and synthesis and secretion of digestive enzymes [75, 76]. Our study has also captured indirect evidence that oxidative stress suppressed antioxidant gene expression and disrupted fatty acid metabolism due to the observation of vacuolation in R-cells. The histoarchitecture of gills in the hypoxia group showed hemocytic infiltration, fused gill lamellae, mild malformations, swollen and necrotic lamellae, and complete disorganization of lamellae (Fig. 6c & d). All these incidents can eventually lead to gill injury, which leads to disturbance in oxygen consumption [77] and enzymatic activities [78] in aquatic organisms. However, no obvious alterations were observed by light microscopy in the muscle tissues of M. nipponense after chronic hypoxia (Fig. 6e & f).Fig. 6

Bottom Line: Oriental river prawn, Macrobrachium nipponense, is a commercially important species found in brackish and fresh waters throughout China.However, the effects of dissolved oxygen availability on gene expression and physiological functions of those tissues of prawns are unknown.Genes from well known functional categories and signaling pathways associated with stress responses and adaptation to extreme environments were significantly enriched, including genes in the functional categories "response to stimulus", "transferase activity" and "oxidoreductase activity", and the signaling pathways "oxidative phosphorylation", "glycolysis/gluconeogenesis" and "MAPK signaling".

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Genetic Breeding and Aquaculture Biology of Freshwater Fishes, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, People's Republic of China. sunshengming621416@163.com.

ABSTRACT

Background: Oriental river prawn, Macrobrachium nipponense, is a commercially important species found in brackish and fresh waters throughout China. Chronic hypoxia is a major physiological challenge for prawns in culture, and the hepatopancreas, muscle and gill tissues play important roles in adaptive processes. However, the effects of dissolved oxygen availability on gene expression and physiological functions of those tissues of prawns are unknown. Adaptation to hypoxia is a complex process, to help us understand stress-sensing mechanism and ultimately permit selection for hypoxia- tolerant prawns, we performed transcriptomic analysis of juvenile M. nipponense hepatopancreas, gill and muscle tissues by RNA-Seq.

Results: Approximately 46,472,741; 52,773,612 and 58,195,908 raw sequence reads were generated from hepatopancreas, muscle and gill tissues, respectively. A total of 62,722 unigenes were generated, of the assembled unigenes, we identified 8,892 genes that were significantly up-regulated, while 5,760 genes were significantly down-regulated in response to chronic hypoxia. Genes from well known functional categories and signaling pathways associated with stress responses and adaptation to extreme environments were significantly enriched, including genes in the functional categories "response to stimulus", "transferase activity" and "oxidoreductase activity", and the signaling pathways "oxidative phosphorylation", "glycolysis/gluconeogenesis" and "MAPK signaling". The expression patterns of 18 DEGs involved in hypoxic regulation of M. nipponense were validated by quantitative real-time reverse-transcriptase polymerase chain reactions (qRT-PCR; average correlation coefficient = 0.94). In addition, the hepatopancreas and gills exhibited histological differences between hypoxia and normoxia groups. These structural alterations could affect the vital physiological functions of prawns in response to chronic hypoxia, which could adversely affect growth and survival of M. nipponense.

Conclusions: Gene expression changes in tissues from the oriental river prawn provide a preliminary basis to better understand the molecular responses of M. nipponense to chronic hypoxia. The differentially expressed genes (DEGs) identified in M. nipponense under hypoxia stress may be important for future genetic improvement of cultivated prawns or other crustaceans through transgenic approaches aimed at increasing hypoxia tolerance.

No MeSH data available.


Related in: MedlinePlus