Evolutionary origins of Pax6 control of crystallin genes

Ales Cvekl, Yilin Zhao, Rebecca S. Estrada, Qing Xie, Xun Gu, Deyou Zheng

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

The birth of novel genes, including their cell-specific transcriptional control, is a major source of evolutionary innovation. The lens-preferred proteins, crystallins (vertebrates: a-and b/c-crystallins), provide a gateway to study eye evolution. Diversity of crystallins was thought to originate from convergent evolution through multiple, independent formation of Pax6/PaxB-binding sites within the promoters of genes able to act as crystallins. Here, we propose that aB-crystallin arose from a duplication of small heat shock protein (Hspb1-like) gene accompanied by Pax6-site and heat shock element (HSE) formation, followed by another duplication to generate the aA-crystallin gene in which HSE was converted into another Pax6-binding site. The founding b/c-crystallin gene arose from the ancestral Hspb1-like gene promoter inserted into a Ca2+-binding protein coding region, early in the cephalochordate/tunicate lineage. Likewise, an ancestral aldehyde dehydrogenase (Aldh) gene, through multiple gene duplications, expanded into a multigene family, with specific genes expressed in invertebrate lenses (X-crystallin/Aldh1a9) and both vertebrate lenses (g-crystallin/Aldh1a7 and Aldh3a1) and corneas (Aldh3a1). Collectively, the present data reconstruct the evolution of diverse crystallin gene families.

Original languageEnglish (US)
Pages (from-to)2075-2092
Number of pages18
JournalGenome Biology and Evolution
Volume9
Issue number8
DOIs
StatePublished - 2017

Fingerprint

crystallins
Crystallins
gene
Genes
genes
heat shock
Lens
protein
heat stress
binding sites
Lenses
vertebrate
Vertebrates
Shock
vertebrates
promoter regions
Hot Temperature
Binding Sites
aldehyde dehydrogenase
convergent evolution

Keywords

  • Aldehyde dehydrogenase
  • Crystallin
  • Eye evolution
  • Heat shock responsive element
  • Lens
  • Pax6
  • Small heat shock protein

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Evolutionary origins of Pax6 control of crystallin genes. / Cvekl, Ales; Zhao, Yilin; Estrada, Rebecca S.; Xie, Qing; Gu, Xun; Zheng, Deyou.

In: Genome Biology and Evolution, Vol. 9, No. 8, 2017, p. 2075-2092.

Research output: Contribution to journalArticle

@article{3a201af628d7404f8b6fc29e7cf91d1d,
title = "Evolutionary origins of Pax6 control of crystallin genes",
abstract = "The birth of novel genes, including their cell-specific transcriptional control, is a major source of evolutionary innovation. The lens-preferred proteins, crystallins (vertebrates: a-and b/c-crystallins), provide a gateway to study eye evolution. Diversity of crystallins was thought to originate from convergent evolution through multiple, independent formation of Pax6/PaxB-binding sites within the promoters of genes able to act as crystallins. Here, we propose that aB-crystallin arose from a duplication of small heat shock protein (Hspb1-like) gene accompanied by Pax6-site and heat shock element (HSE) formation, followed by another duplication to generate the aA-crystallin gene in which HSE was converted into another Pax6-binding site. The founding b/c-crystallin gene arose from the ancestral Hspb1-like gene promoter inserted into a Ca2+-binding protein coding region, early in the cephalochordate/tunicate lineage. Likewise, an ancestral aldehyde dehydrogenase (Aldh) gene, through multiple gene duplications, expanded into a multigene family, with specific genes expressed in invertebrate lenses (X-crystallin/Aldh1a9) and both vertebrate lenses (g-crystallin/Aldh1a7 and Aldh3a1) and corneas (Aldh3a1). Collectively, the present data reconstruct the evolution of diverse crystallin gene families.",
keywords = "Aldehyde dehydrogenase, Crystallin, Eye evolution, Heat shock responsive element, Lens, Pax6, Small heat shock protein",
author = "Ales Cvekl and Yilin Zhao and Estrada, {Rebecca S.} and Qing Xie and Xun Gu and Deyou Zheng",
year = "2017",
doi = "10.1093/gbe/evx153",
language = "English (US)",
volume = "9",
pages = "2075--2092",
journal = "Genome Biology and Evolution",
issn = "1759-6653",
publisher = "Oxford University Press",
number = "8",

}

TY - JOUR

T1 - Evolutionary origins of Pax6 control of crystallin genes

AU - Cvekl, Ales

AU - Zhao, Yilin

AU - Estrada, Rebecca S.

AU - Xie, Qing

AU - Gu, Xun

AU - Zheng, Deyou

PY - 2017

Y1 - 2017

N2 - The birth of novel genes, including their cell-specific transcriptional control, is a major source of evolutionary innovation. The lens-preferred proteins, crystallins (vertebrates: a-and b/c-crystallins), provide a gateway to study eye evolution. Diversity of crystallins was thought to originate from convergent evolution through multiple, independent formation of Pax6/PaxB-binding sites within the promoters of genes able to act as crystallins. Here, we propose that aB-crystallin arose from a duplication of small heat shock protein (Hspb1-like) gene accompanied by Pax6-site and heat shock element (HSE) formation, followed by another duplication to generate the aA-crystallin gene in which HSE was converted into another Pax6-binding site. The founding b/c-crystallin gene arose from the ancestral Hspb1-like gene promoter inserted into a Ca2+-binding protein coding region, early in the cephalochordate/tunicate lineage. Likewise, an ancestral aldehyde dehydrogenase (Aldh) gene, through multiple gene duplications, expanded into a multigene family, with specific genes expressed in invertebrate lenses (X-crystallin/Aldh1a9) and both vertebrate lenses (g-crystallin/Aldh1a7 and Aldh3a1) and corneas (Aldh3a1). Collectively, the present data reconstruct the evolution of diverse crystallin gene families.

AB - The birth of novel genes, including their cell-specific transcriptional control, is a major source of evolutionary innovation. The lens-preferred proteins, crystallins (vertebrates: a-and b/c-crystallins), provide a gateway to study eye evolution. Diversity of crystallins was thought to originate from convergent evolution through multiple, independent formation of Pax6/PaxB-binding sites within the promoters of genes able to act as crystallins. Here, we propose that aB-crystallin arose from a duplication of small heat shock protein (Hspb1-like) gene accompanied by Pax6-site and heat shock element (HSE) formation, followed by another duplication to generate the aA-crystallin gene in which HSE was converted into another Pax6-binding site. The founding b/c-crystallin gene arose from the ancestral Hspb1-like gene promoter inserted into a Ca2+-binding protein coding region, early in the cephalochordate/tunicate lineage. Likewise, an ancestral aldehyde dehydrogenase (Aldh) gene, through multiple gene duplications, expanded into a multigene family, with specific genes expressed in invertebrate lenses (X-crystallin/Aldh1a9) and both vertebrate lenses (g-crystallin/Aldh1a7 and Aldh3a1) and corneas (Aldh3a1). Collectively, the present data reconstruct the evolution of diverse crystallin gene families.

KW - Aldehyde dehydrogenase

KW - Crystallin

KW - Eye evolution

KW - Heat shock responsive element

KW - Lens

KW - Pax6

KW - Small heat shock protein

UR - http://www.scopus.com/inward/record.url?scp=85032006787&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85032006787&partnerID=8YFLogxK

U2 - 10.1093/gbe/evx153

DO - 10.1093/gbe/evx153

M3 - Article

VL - 9

SP - 2075

EP - 2092

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 8

ER -