Genomics comparisons of three chromosome-level mudskipper genome assemblies reveal molecular clues for water-to-land evolution and adaptation,Journal of Advanced Research

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Genomics comparisons of three chromosome-level mudskipper genome assemblies reveal molecular clues for water-to-land evolution and adaptation
Journal of Advanced Research ( IF 11.4 ) Pub Date : 2023-05-21 , DOI: 10.1016/j.jare.2023.05.005
Chao Bian ₁ , Yu Huang ₂ , Ruihan Li ₃ , Pengwei Xu ₃ , Xinxin You ₄ , Yunyun Lv ₅ , Zhiqiang Ruan ₄ , Jieming Chen ₄ , Junmin Xu ₄ , Qiong Shi ₆

Affiliation

Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China; Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang 641100, China.
Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China.
Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China.
Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China; Applied Research Institute for Modern Fishery Industry, Guangdong Dabaihui Marine Technology Group Co. Ltd., Huizhou 516357, China.
Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang 641100, China.
Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China; Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, China; Key Laboratory of Sichuan Province for Fishes Conservation and Utilization in the Upper Reaches of the Yangtze River, College of Life Sciences, Neijiang Normal University, Neijiang 641100, China; Applied Research Institute for Modern Fishery Industry, Guangdong Dabaihui Marine Technology Group Co. Ltd., Huizhou 516357, China.

Mudskippers are a large group of amphibious fishes that have developed many morphological and physiological capacities to live on land. Genomics comparisons of chromosome-level genome assemblies of three representative mudskippers, (BP), (PM) and (PMO), may be able to provide novel insights into the water-to-land evolution and adaptation. Two chromosome-level genome assemblies for BP and PM were respectively sequenced by an integration of PacBio, Nanopore and Hi-C sequencing. A series of standard assembly and annotation pipelines were subsequently performed for both mudskippers. We also re-annotated the PMO genome, downloaded from NCBI, to obtain a redundancy-reduced annotation. Three-way comparative analyses of the three mudskipper genomes in a large scale were carried out to discover detailed genomic differences, such as different gene sizes, and potential chromosomal fission and fusion events. Comparisons of several representative gene families among the three amphibious mudskippers and some other teleosts were also performed to find some molecular clues for terrestrial adaptation. We obtained two high-quality haplotype genome assemblies with 23 and 25 chromosomes for BP and PM respectively. We also found two specific chromosome fission events in PM. Ancestor chromosome analysis has discovered a common fusion event in mudskipper ancestor. This fusion was then retained in all the three mudskipper species. A loss of some (secretory calcium-binding phosphoprotein) genes were identified in the three mudskipper genomes, which could lead to reduction of scales for a part-time terrestrial residence. The loss of gene, encoding an important enzyme (arylalkylamine N-acetyltransferase 1a, AANAT1a) for dopamine metabolism and melatonin biosynthesis, was confirmed in PM but not in PMO (as previously reported existence in BP), suggesting a better air vision of PM than both PMO and BP. Such a tiny variation within the genus exemplifies to prove a step-by-step evolution for the mudskippers’ water-to-land adaptation. These high-quality mudskipper genome assemblies will become valuable genetic resources for in-depth discovery of genomic evolution for the terrestrial adaptation of amphibious fishes.

中文翻译：

三个染色体水平弹涂鱼基因组组装的基因组比较揭示了水陆进化和适应的分子线索

弹涂鱼是一大类两栖鱼类，它们已经发展出许多在陆地上生活的形态和生理能力。对三种代表性弹涂鱼 (BP)、(PM) 和 (PMO) 的染色体水平基因组组装进行基因组比较，可能能够为从水到陆地的进化和适应提供新的见解。 BP 和 PM 的两个染色体水平基因组组装体分别通过 PacBio、Nanopore 和 Hi-C 测序的整合进行测序。随后为两个弹涂鱼执行了一系列标准组装和注释管道。我们还重新注释了从 NCBI 下载的 PMO 基因组，以获得冗余减少的注释。对三种弹涂鱼基因组进行了大规模的三向比较分析，以发现详细的基因组差异，例如不同的基因大小以及潜在的染色体裂变和融合事件。还对三种两栖弹涂鱼和其他一些硬骨鱼之间的几个代表性基因家族进行了比较，以寻找陆地适应的一些分子线索。我们获得了两个高质量的单倍型基因组组装体，分别具有 BP 和 PM 的 23 和 25 条染色体。我们还在 PM 中发现了两个特定的染色体裂变事件。祖先染色体分析发现弹涂鱼祖先中有一个共同的融合事件。这种融合随后被保留在所有三种弹涂鱼物种中。在三个弹涂鱼基因组中发现了一些（分泌性钙结合磷蛋白）基因的丢失，这可能导致兼职陆地居住的规模减少。编码多巴胺代谢和褪黑素生物合成的重要酶（芳烷基胺 N-乙酰转移酶 1a，AANAT1a）的基因缺失在 PM 中得到证实，但在 PMO 中没有得到证实（正如之前报道的 BP 中存在的那样），这表明 PM 的空气视力比 PM 更好PMO 和 BP。该属内如此微小的变异证明了弹涂鱼从水到陆地的适应是逐步进化的。这些高质量的弹涂鱼基因组组合将成为深入发现两栖鱼类陆地适应的基因组进化的宝贵遗传资源。

更新日期：2023-05-21

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