Genome architecture drives protein evolution in ciliates

被引:62
|
作者
Zufall, Rebecca A.
McGrath, Casey L.
Muse, Spencer V.
Katz, Laura A.
机构
[1] Smith Coll, Dept Biol Sci, Northampton, MA 01063 USA
[2] N Carolina State Univ, Dept Stat, Raleigh, NC 27695 USA
[3] N Carolina State Univ, Bioinformat Res Ctr, Raleigh, NC 27695 USA
[4] Univ Massachusetts, Program Organism & Evolutionary Biol, Amherst, MA 01003 USA
关键词
genome evolution; genome architecture; protein evolution; ciliate evolution;
D O I
10.1093/molbev/msl032
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Studies of microbial eukaryotes have been pivotal in the discovery of biological phenomena, including RNA editing, self-splicing RNA, and telomere addition. Here we extend this list by demonstrating that genome architecture, namely the extensive processing of somatic (macronuclear) genomes in some ciliate lineages, is associated with elevated rates of protein evolution. Using newly developed likelihood-based procedures for studying molecular evolution, we investigate 6 genes to compare 1) ciliate protein evolution to that of 3 other clades of eukaryotes (plants, animals, and fungi) and 2) protein evolution in ciliates with extensively processed macronuclear genomes to that of other ciliate lineages. In 5 of the 6 genes, ciliates are estimated to have a higher ratio of nonsynonymous/synonymous substitution rates, consistent with an increase in the rate of protein diversification in ciliates relative to other eukaryotes. Even more striking, there is a significant effect of genome architecture within ciliates as the most divergent proteins are consistently found in those lineages with the most highly processed macronuclear genomes. We propose a model whereby genome architecture-specifically chromosomal processing, amitosis within macronuclei, and epigenetics-allows ciliates to explore protein space in a novel manner. Further, we predict that examination of diverse eukaryotes will reveal additional evidence of the impact of genome architecture on molecular evolution.
引用
收藏
页码:1681 / 1687
页数:7
相关论文
共 50 条
  • [1] Evolutionary origins and impacts of genome architecture in ciliates
    Maurer-Alcala, Xyrus X.
    Nowacki, Mariusz
    ANNALS OF THE NEW YORK ACADEMY OF SCIENCES, 2019, 1447 (01) : 110 - 118
  • [2] PHOSPHORUS DRIVES THE EVOLUTION OF NEMATODE LIFE HISTORY TRAITS AND GENOME ARCHITECTURE
    Adams, Byron J.
    Xue, X.
    Adhikari, B.
    Simmons, Breana
    Ball, B.
    Barrett, J.
    Perkes, A.
    Martin, M.
    Wall, D. H.
    JOURNAL OF NEMATOLOGY, 2018, 50 (04) : 624 - 624
  • [3] Mitogenomic architecture and evolution of the soil ciliates Colpoda
    Zhang, Yuanyuan
    Li, Haichao
    Wang, Yaohai
    Nie, Mu
    Zhang, Kexin
    Pan, Jiao
    Zhang, Yu
    Ye, Zhiqiang
    Zufall, Rebecca A.
    Lynch, Michael
    Long, Hongan
    MSYSTEMS, 2024, 9 (02)
  • [4] Transposon proliferation drives genome architecture and regulatory evolution in wild and domesticated peppers
    Zhang, Kang
    Yu, Hailong
    Zhang, Lingkui
    Cao, Yacong
    Li, Xing
    Mei, Yajie
    Wang, Xiang
    Zhang, Zhenghai
    Li, Tianyao
    Jin, Yuan
    Fan, Wenyuan
    Guan, Congcong
    Wang, Yihan
    Zhou, Daiyuan
    Chen, Shumin
    Wu, Huamao
    Wang, Lihao
    Cheng, Feng
    NATURE PLANTS, 2025, : 359 - 375
  • [5] Somatic genome architecture and molecular evolution are decoupled in "young" linage-specific gene families in ciliates
    Maurer-Alcala, Xyrus X.
    Cote-L'Heureux, Auden
    Pond, Sergei L. Kosakovsky
    Katz, Laura A.
    PLOS ONE, 2024, 19 (01):
  • [6] Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates
    Yan, Ying
    Maurer-Alcala, Xyrus X.
    Knight, Rob
    Pond, Sergei L. Kosakovsky
    Katz, Laura A.
    MBIO, 2019, 10 (06):
  • [7] Evolution of genome architecture
    Koonin, Eugene V.
    INTERNATIONAL JOURNAL OF BIOCHEMISTRY & CELL BIOLOGY, 2009, 41 (02): : 298 - 306
  • [8] Genome heterogeneity drives the evolution of species
    Miotto, Mattia
    Monacelli, Lorenzo
    PHYSICAL REVIEW RESEARCH, 2020, 2 (04):
  • [9] GENOME STRUCTURE DRIVES PATTERNS OF GENE FAMILY EVOLUTION IN CILIATES, A CASE STUDY USING CHILODONELLA UNCINATA (PROTISTA, CILIOPHORA, PHYLLOPHARYNGEA)
    Gao, Feng
    Song, Weibo
    Katz, Laura A.
    EVOLUTION, 2014, 68 (08) : 2287 - 2295
  • [10] Genome gymnastics: Unique modes of DNA evolution and processing in ciliates
    Prescott, DM
    NATURE REVIEWS GENETICS, 2000, 1 (03) : 191 - 198