Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth

Proc Natl Acad Sci U S A. 2009 Aug 11;106(32):13341-6. doi: 10.1073/pnas.0901170106. Epub 2009 Jul 24.

Abstract

Formins are present in all eukaryotes and are essential for the creation of actin-based structures responsible for diverse cellular processes. Because multicellular organisms contain large formin gene families, establishing the physiological functions of formin isoforms has been difficult. Using RNAi, we analyzed the function of all 9 formin genes within the moss Physcomitrella patens. We show that plants lacking class II formins (For2) are severely stunted and composed of spherical cells with disrupted actin organization. In contrast, silencing of all other formins results in normal elongated cell morphology and actin organization. Consistent with a role in polarized growth, For2 are apically localized in growing cells. We show that an N-terminal phosphatase tensin (PTEN)-like domain mediates apical localization. The PTEN-like domain is followed by a conserved formin homology (FH)1-FH2 domain, known to promote actin polymerization. To determine whether apical localization of any FH1-FH2 domain mediates polarized growth, we performed domain swapping. We found that only the class II FH1-FH2, in combination with the PTEN-like domain, rescues polarized growth, because it cannot be replaced with a similar domain from a For1. We used in vitro polymerization assays to dissect the functional differences between these FH1-FH2 domains. We found that both the FH1 and the FH2 domains from For2 are required to mediate exceptionally rapid rates of actin filament elongation, much faster than any other known formin. Thus, our data demonstrate that rapid rates of actin elongation are critical for driving the formation of apical filamentous actin necessary for polarized growth.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actins / metabolism
  • Bryopsida / anatomy & histology
  • Bryopsida / cytology*
  • Bryopsida / growth & development*
  • Cell Polarity
  • Fetal Proteins / chemistry
  • Fetal Proteins / metabolism
  • Formins
  • Gene Silencing
  • Genetic Complementation Test
  • Microfilament Proteins / chemistry
  • Microfilament Proteins / metabolism
  • Molecular Sequence Data
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / metabolism*
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / metabolism
  • PTEN Phosphohydrolase / chemistry
  • Protein Isoforms / chemistry
  • Protein Isoforms / metabolism
  • Protein Structure, Tertiary
  • Protein Transport

Substances

  • Actins
  • Fetal Proteins
  • Formins
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Protein Isoforms
  • PTEN Phosphohydrolase

Associated data

  • GENBANK/FJ997271
  • GENBANK/FJ997272