Evolution of early embryogenesis in rhabditid nematodes

Michael Brauchle, Karin Kiontke, Philip MacMenamin, David H A Fitch, Fabio Piano

Research output: Contribution to journalArticle

Abstract

The cell-biological events that guide early-embryonic development occur with great precision within species but can be quite diverse across species. How these cellular processes evolve and which molecular components underlie evolutionary changes is poorly understood. To begin to address these questions, we systematically investigated early embryogenesis, from the one- to the four-cell embryo, in 34 nematode species related to C. elegans. We found 40 cell-biological characters that captured the phenotypic differences between these species. By tracing the evolutionary changes on a molecular phylogeny, we found that these characters evolved multiple times and independently of one another. Strikingly, all these phenotypes are mimicked by single-gene RNAi experiments in C. elegans. We use these comparisons to hypothesize the molecular mechanisms underlying the evolutionary changes. For example, we predict that a cell polarity module was altered during the evolution of the Protorhabditis group and show that PAR-1, a kinase localized asymmetrically in C. elegans early embryos, is symmetrically localized in the one-cell stage of Protorhabditis group species. Our genome-wide approach identifies candidate molecules-and thereby modules-associated with evolutionary changes in cell-biological phenotypes.

Original languageEnglish (US)
Pages (from-to)253-262
Number of pages10
JournalDevelopmental Biology
Volume335
Issue number1
DOIs
StatePublished - Nov 1 2009

Fingerprint

Embryonic Development
Embryonic Structures
Phenotype
Cell Polarity
Phylogeny
RNA Interference
Phosphotransferases
Genome
Genes

Keywords

  • C. elegans
  • Cell polarity
  • Early development
  • Embryogenesis
  • Nematoda
  • Phenotypic analysis
  • Phenotypic plasticity

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology
  • Molecular Biology

Cite this

Evolution of early embryogenesis in rhabditid nematodes. / Brauchle, Michael; Kiontke, Karin; MacMenamin, Philip; Fitch, David H A; Piano, Fabio.

In: Developmental Biology, Vol. 335, No. 1, 01.11.2009, p. 253-262.

Research output: Contribution to journalArticle

Brauchle, Michael ; Kiontke, Karin ; MacMenamin, Philip ; Fitch, David H A ; Piano, Fabio. / Evolution of early embryogenesis in rhabditid nematodes. In: Developmental Biology. 2009 ; Vol. 335, No. 1. pp. 253-262.
@article{a53e93c5974f403fbb4dc4bc41e4ef91,
title = "Evolution of early embryogenesis in rhabditid nematodes",
abstract = "The cell-biological events that guide early-embryonic development occur with great precision within species but can be quite diverse across species. How these cellular processes evolve and which molecular components underlie evolutionary changes is poorly understood. To begin to address these questions, we systematically investigated early embryogenesis, from the one- to the four-cell embryo, in 34 nematode species related to C. elegans. We found 40 cell-biological characters that captured the phenotypic differences between these species. By tracing the evolutionary changes on a molecular phylogeny, we found that these characters evolved multiple times and independently of one another. Strikingly, all these phenotypes are mimicked by single-gene RNAi experiments in C. elegans. We use these comparisons to hypothesize the molecular mechanisms underlying the evolutionary changes. For example, we predict that a cell polarity module was altered during the evolution of the Protorhabditis group and show that PAR-1, a kinase localized asymmetrically in C. elegans early embryos, is symmetrically localized in the one-cell stage of Protorhabditis group species. Our genome-wide approach identifies candidate molecules-and thereby modules-associated with evolutionary changes in cell-biological phenotypes.",
keywords = "C. elegans, Cell polarity, Early development, Embryogenesis, Nematoda, Phenotypic analysis, Phenotypic plasticity",
author = "Michael Brauchle and Karin Kiontke and Philip MacMenamin and Fitch, {David H A} and Fabio Piano",
year = "2009",
month = "11",
day = "1",
doi = "10.1016/j.ydbio.2009.07.033",
language = "English (US)",
volume = "335",
pages = "253--262",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "1",

}

TY - JOUR

T1 - Evolution of early embryogenesis in rhabditid nematodes

AU - Brauchle, Michael

AU - Kiontke, Karin

AU - MacMenamin, Philip

AU - Fitch, David H A

AU - Piano, Fabio

PY - 2009/11/1

Y1 - 2009/11/1

N2 - The cell-biological events that guide early-embryonic development occur with great precision within species but can be quite diverse across species. How these cellular processes evolve and which molecular components underlie evolutionary changes is poorly understood. To begin to address these questions, we systematically investigated early embryogenesis, from the one- to the four-cell embryo, in 34 nematode species related to C. elegans. We found 40 cell-biological characters that captured the phenotypic differences between these species. By tracing the evolutionary changes on a molecular phylogeny, we found that these characters evolved multiple times and independently of one another. Strikingly, all these phenotypes are mimicked by single-gene RNAi experiments in C. elegans. We use these comparisons to hypothesize the molecular mechanisms underlying the evolutionary changes. For example, we predict that a cell polarity module was altered during the evolution of the Protorhabditis group and show that PAR-1, a kinase localized asymmetrically in C. elegans early embryos, is symmetrically localized in the one-cell stage of Protorhabditis group species. Our genome-wide approach identifies candidate molecules-and thereby modules-associated with evolutionary changes in cell-biological phenotypes.

AB - The cell-biological events that guide early-embryonic development occur with great precision within species but can be quite diverse across species. How these cellular processes evolve and which molecular components underlie evolutionary changes is poorly understood. To begin to address these questions, we systematically investigated early embryogenesis, from the one- to the four-cell embryo, in 34 nematode species related to C. elegans. We found 40 cell-biological characters that captured the phenotypic differences between these species. By tracing the evolutionary changes on a molecular phylogeny, we found that these characters evolved multiple times and independently of one another. Strikingly, all these phenotypes are mimicked by single-gene RNAi experiments in C. elegans. We use these comparisons to hypothesize the molecular mechanisms underlying the evolutionary changes. For example, we predict that a cell polarity module was altered during the evolution of the Protorhabditis group and show that PAR-1, a kinase localized asymmetrically in C. elegans early embryos, is symmetrically localized in the one-cell stage of Protorhabditis group species. Our genome-wide approach identifies candidate molecules-and thereby modules-associated with evolutionary changes in cell-biological phenotypes.

KW - C. elegans

KW - Cell polarity

KW - Early development

KW - Embryogenesis

KW - Nematoda

KW - Phenotypic analysis

KW - Phenotypic plasticity

UR - http://www.scopus.com/inward/record.url?scp=70349288116&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70349288116&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2009.07.033

DO - 10.1016/j.ydbio.2009.07.033

M3 - Article

VL - 335

SP - 253

EP - 262

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 1

ER -