The habu genome reveals accelerated evolution of venom protein genes

Hiroki Shibata,Hitomi Nakamura,Kosuke Tashiro,Yoichi Matsuda,Hironobu Goto ,Kazuki Mori,Satoru Kuhara,Motonori Ohno,Kazuaki Yamaguchi,Kanako Hisata,Eiichi Shoguchi,Manabu Fujie,Shin‐Ichi Yamasaki ,Shousaku Hattori,Kazumi Matsubara,Akiko Isomoto,Ryo Koyanagi,Takeshi Takeuchi,Takahito Chijiwa,Naoko Oda-Ueda,Noriyuki Satoh,Yasuyuki Fukumaki,Akifumi Yamashita,Tomoya Ogawa

doi:10.1038/s41598-018-28749-4

Abstract

Evolution of novel traits is a challenging subject in biological research. Several snake lineages developed elaborate venom systems to deliver complex protein mixtures for prey capture. To understand mechanisms involved in snake venom evolution, we decoded here the ~1.4-Gb genome of a habu, Protobothrops flavoviridis. We identified 60 snake venom protein genes (SV) and 224 non-venom paralogs (NV), belonging to 18 gene families. Molecular phylogeny reveals early divergence of SV and NV genes, suggesting that one of the four copies generated through two rounds of whole-genome duplication was modified for use as a toxin. Among them, both SV and NV genes in four major components were extensively duplicated after their diversification, but accelerated evolution is evident exclusively in the SV genes. Both venom-related SV and NV genes are significantly enriched in microchromosomes. The present study thus provides a genetic background for evolution of snake venom composition.

Highlights

Evolution of novel traits is a challenging subject in biological research
To what extent did venom genes duplicate? What sorts of alternative splicing are involved in diversification of venom genes? Did two-rounds of whole genome duplication (2R-WGD) that occurred in the vertebrate lineage contribute to the modification of ancestral genes to produce toxic protein variants? Are duplicated gene copies scattered throughout the genome or clustered in certain chromosomal regions? If so, do macrochromosomes (MACs) or microchromosomes (MICs) host the cluster? To address these questions, we sequenced the genome of the habu, P. flavoviridis, and comprehensively analyzed genes encoding venom (SV) and paralogous, non-venom proteins (NV)
The quality and completeness of the genome assembly were assessed by searching for a set of 233 core vertebrate genes using BUSCO v214 implemented in gVolante[15]

Summary

Introduction

Evolution of novel traits is a challenging subject in biological research. Several snake lineages developed elaborate venom systems to deliver complex protein mixtures for prey capture. Molecular phylogeny reveals early divergence of SV and NV genes, suggesting that one of the four copies generated through two rounds of wholegenome duplication was modified for use as a toxin Among them, both SV and NV genes in four major components were extensively duplicated after their diversification, but accelerated evolution is evident exclusively in the SV genes. Recent analyses of high-throughput transcriptomics have shown highly divergent venom profiles[9,10,11] Despite such extensive studies, the evolutionary origins of snake venom proteins and the genetic bases of venom diversity are as yet poorly understood.

Methods

Results

Conclusion