Deciphering the genetic programme triggering timely and spatially-regulated chitin deposition

PLoS Genet. 2015 Jan 24;11(1):e1004939. doi: 10.1371/journal.pgen.1004939. eCollection 2015 Jan.

Abstract

Organ and tissue formation requires a finely tuned temporal and spatial regulation of differentiation programmes. This is necessary to balance sufficient plasticity to undergo morphogenesis with the acquisition of the mature traits needed for physiological activity. Here we addressed this issue by analysing the deposition of the chitinous extracellular matrix of Drosophila, an essential element of the cuticle (skin) and respiratory system (tracheae) in this insect. Chitin deposition requires the activity of the chitin synthase Krotzkopf verkehrt (Kkv). Our data demonstrate that this process equally requires the activity of two other genes, namely expansion (exp) and rebuf (reb). We found that Exp and Reb have interchangeable functions, and in their absence no chitin is produced, in spite of the presence of Kkv. Conversely, when Kkv and Exp/Reb are co-expressed in the ectoderm, they promote chitin deposition, even in tissues normally devoid of this polysaccharide. Therefore, our results indicate that both functions are not only required but also sufficient to trigger chitin accumulation. We show that this mechanism is highly regulated in time and space, ensuring chitin accumulation in the correct tissues and developmental stages. Accordingly, we observed that unregulated chitin deposition disturbs morphogenesis, thus highlighting the need for tight regulation of this process. In summary, here we identify the genetic programme that triggers the timely and spatially regulated deposition of chitin and thus provide new insights into the extracellular matrix maturation required for physiological activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Chitin / biosynthesis*
  • Chitin / genetics
  • Chitin Synthase / genetics*
  • Chitin Synthase / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Embryonic Development / genetics*
  • Extracellular Matrix / genetics
  • Gene Expression Regulation, Developmental
  • Morphogenesis
  • Phenotype
  • Trachea / enzymology
  • Trachea / growth & development

Substances

  • Drosophila Proteins
  • Chitin
  • kkv protein, Drosophila
  • Chitin Synthase

Grant support

This work was supported by Ministerio de Economía y Competitividad of the Spanish Government (BFU2009-09041/BMC, BFU2012-39509-C02 and Programme Consolider CSD2007-00008), and from AGAUR of the Generalitat de Catalunya (2009 SGR1333) to ML and from German Research Foundation (MO1714/2-2 and 3-2) to BM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.