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Genome-wide identification and characterization of heat shock protein family 70 provides insight into its divergent functions on immune response and development of Paralichthys olivaceus

Liu, Kaiqiang, Hao, Xiancai, Wang, Qian, Hou, Jilun, Lai, Xiaofang, Dong, Zhiguo, Shao, Changwei·2019·PeerJ
DOI 10.7717/peerj.7781PMC PMC6855204
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Abstract

Flatfish undergo extreme morphological development and settle to a benthic in the adult stage, and are likely to be more susceptible to environmental stress. Heat shock proteins 70 ( hsp70 ) are involved in embryonic development and stress response in metazoan animals. However, the evolutionary history and functions of hsp70 in flatfish are poorly understood. Here, we identified 15 hsp70 genes in the genome of Japanese flounder ( Paralichthys olivaceus ), a flatfish endemic to northwestern Pacific Ocean. Gene structure and motifs of the Japanese flounder hsp70 were conserved, and there were few structure variants compared to other fish species. We constructed a maximum likelihood tree to understand the evolutionary relationship of the hsp70 genes among surveyed fish. Selection pressure analysis suggested that four genes, hspa4l , hspa9 , hspa13, and hyou1 , showed signs of positive selection. We then extracted transcriptome data on the Japanese flounder with Edwardsiella tarda to induce stress, and found that hspa9 , hspa12b, hspa4l, hspa13 , and hyou1 were highly expressed, likely to protect cells from stress. Interestingly, expression patterns of hsp70 genes were divergent in different developmental stages of the Japanese flounder. We found that at least one hsp70 gene was always highly expressed at various stages of embryonic development of the Japanese flounder, thereby indicating that hsp70 genes were constitutively expressed in the Japanese flounder. Our findings provide basic and useful resources to better understand hsp70 genes in flatfish.

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Figure 1 Phylogenetic tree of hsp70 from flounder, medaka, tilapia, zebrafish, platyfish, tetraodon, and stickleback. The color in the background indicates the branch of sub-family and corresponds to the sub-family names marked in the same color as the circle beyond. The hsp70 genes from flounder are marked with a red star.
Figure 1 Phylogenetic tree of hsp70 from flounder, medaka, tilapia, zebrafish, platyfish, tetraodon, and stickleback. The color in the background indicates the branch of sub-family and corresponds to the sub-family names marked in the same color as the circle beyond. The hsp70 genes from flounder are marked with a red star.CC BY · PubMed Central
Figure 2 Intron-exon structure of hsp70 genes in flounder. The phylogenetic tree on the left panel was generated using MEGA7 with the Neighbor-joining (NJ) method and 1,000 bootstrap replicates. The right of the panel shows exon and intron structure of hsp70, where the orange rectangles represent exons, black polylines indicate introns, orange and black line indicates scale.
Figure 2 Intron-exon structure of hsp70 genes in flounder. The phylogenetic tree on the left panel was generated using MEGA7 with the Neighbor-joining (NJ) method and 1,000 bootstrap replicates. The right of the panel shows exon and intron structure of hsp70, where the orange rectangles represent exons, black polylines indicate introns, orange and black line indicates scale.CC BY · PubMed Central
Figure 3 Schematic representation of conserved motifs in HSP70 proteins. Each colored box represents a motif and boxes in the same color indicate the same motif.
Figure 3 Schematic representation of conserved motifs in HSP70 proteins. Each colored box represents a motif and boxes in the same color indicate the same motif.CC BY · PubMed Central
Figure 4 Multiple alignments of positively selected sites in hspa4l (A) and hspa13 (B). The amino acid residue in the red square represents the positively selective site. The secondary structure was predicted by PHYER2, and α-helixes were indicated in yellow and β-sheets were indicated in blue. The number on the top indicates the position of the amino acid residue in the protein.
Figure 4 Multiple alignments of positively selected sites in hspa4l (A) and hspa13 (B). The amino acid residue in the red square represents the positively selective site. The secondary structure was predicted by PHYER2, and α-helixes were indicated in yellow and β-sheets were indicated in blue. The number on the top indicates the position of the amino acid residue in the protein.CC BY · PubMed Central
Figure 5 The 3D-structural models of HSPA4L (A) and HSPA13 (B). The amino acid under positive selection in HSPA4L is indicated in black (Cys 235) and located in an α-helix. The site under positive selection in HSPA13 is indicated in orange(His 337) and located in a β-sheet.
Figure 5 The 3D-structural models of HSPA4L (A) and HSPA13 (B). The amino acid under positive selection in HSPA4L is indicated in black (Cys 235) and located in an α-helix. The site under positive selection in HSPA13 is indicated in orange(His 337) and located in a β-sheet.CC BY · PubMed Central
Figure 6 Expression patterns hsp70 in Japanese flounder. Each column represents a time point, and each row represents a gene. The relative expression level is indicated by the color bar on the top right. 0 h represents the blank control group at the beginning of the experiment, C 8 h, and C 48 h indicates Ringer’s solution control group, whereas E 8h and 48 h indicate a bacteria-challenged experimental group.
Figure 6 Expression patterns hsp70 in Japanese flounder. Each column represents a time point, and each row represents a gene. The relative expression level is indicated by the color bar on the top right. 0 h represents the blank control group at the beginning of the experiment, C 8 h, and C 48 h indicates Ringer’s solution control group, whereas E 8h and 48 h indicate a bacteria-challenged experimental group.CC BY · PubMed Central
Figure 7 Expression profiles of hspa4l, hsp4a, hspa9, hsc70, hspa1a, hspa8b, hspa13, hspa4b, hsp8a and hspa1b during the life cycle of the Japanese flounder. The panel is split into three parts by the three bars on the top, from left to right represents the germ cells, embryonic development stages, and mature gonads. The detailed stages are oocyte, sperm cell, 4 cell stage, 32 cell stage, 128 cell stage, high blastula, low blastula, early gastrula, late gastrula, myomere stage, heart beat stage, hatch stage, testis, and ovary stage. The relative expression level is indicated by the color bar on the top right.
Figure 7 Expression profiles of hspa4l, hsp4a, hspa9, hsc70, hspa1a, hspa8b, hspa13, hspa4b, hsp8a and hspa1b during the life cycle of the Japanese flounder. The panel is split into three parts by the three bars on the top, from left to right represents the germ cells, embryonic development stages, and mature gonads. The detailed stages are oocyte, sperm cell, 4 cell stage, 32 cell stage, 128 cell stage, high blastula, low blastula, early gastrula, late gastrula, myomere stage, heart beat stage, hatch stage, testis, and ovary stage. The relative expression level is indicated by the color bar on the top right.CC BY · PubMed Central

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Metadata

Authors
Liu, K., Hao, X., Wang, Q., Hou, J., Lai, X., Dong, Z., & Shao, C.
Venue
PeerJ
Publisher
PeerJ
Published
2019-11-11
Volume
7
Pages
e7781
ISSN
2167-8359
DOI
10.7717/peerj.7781
PMC
PMC6855204
Cited by
22
References
1
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (unspecified)
Funders
  • National Key R&D Program of China (2018YFD0900301)
  • Qingdao National Laboratory for Marine Science and Technology (2017ASTCP-ES06)
  • Taishan Scholar Project Fund of Shandong of China
  • National Ten-Thousands Talents Special Support Program
  • The International Scientific Partnership Program ISPP at King Saud University for funding this research work through ISPP No. 0050

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