Local evolution of seed flotation in Arabidopsis

PLoS Genet. 2014 Mar 13;10(3):e1004221. doi: 10.1371/journal.pgen.1004221. eCollection 2014 Mar.

Abstract

Arabidopsis seeds rapidly release hydrophilic polysaccharides from the seed coat on imbibition. These form a heavy mucilage layer around the seed that makes it sink in water. Fourteen natural Arabidopsis variants from central Asia and Scandinavia were identified with seeds that have modified mucilage release and float. Four of these have a novel mucilage phenotype with almost none of the released mucilage adhering to the seed and the absence of cellulose microfibrils. Mucilage release was modified in the variants by ten independent causal mutations in four different loci. Seven distinct mutations affected one locus, coding the MUM2 β-D-galactosidase, and represent a striking example of allelic heterogeneity. The modification of mucilage release has thus evolved a number of times independently in two restricted geographical zones. All the natural mutants identified still accumulated mucilage polysaccharides in seed coat epidermal cells. Using nuclear magnetic resonance (NMR) relaxometry their production and retention was shown to reduce water mobility into internal seed tissues during imbibition, which would help to maintain seed buoyancy. Surprisingly, despite released mucilage being an excellent hydrogel it did not increase the rate of water uptake by internal seed tissues and is more likely to play a role in retaining water around the seed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Evolution, Molecular
  • Magnetic Resonance Spectroscopy
  • Mutation
  • Plant Mucilage / genetics
  • Seeds / genetics
  • Seeds / growth & development*
  • Water / chemistry
  • Water / metabolism
  • beta-Galactosidase / genetics*

Substances

  • Arabidopsis Proteins
  • Plant Mucilage
  • Water
  • beta-Galactosidase

Grants and funding

This work was supported in part by the INRA Plant Biology and Amelioration section (grant number BAP2013_22- ExMu), the ANR-program (grant number ANR-08-BLAN-0061) that included a doctoral fellowship to SSA, and by a doctoral fellowship from the French Ministry of Education and Research to AM. The Zeiss 710 confocal microscope in the IJPB Observatoire du Végétal was cofinanced by a grant from the Conseil Général des Yvelines. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.