Evolution of the bHLH genes involved in stomatal development: implications for the expansion of developmental complexity of stomata in land plants

PLoS One. 2013 Nov 11;8(11):e78997. doi: 10.1371/journal.pone.0078997. eCollection 2013.

Abstract

Stomata play significant roles in plant evolution. A trio of closely related basic Helix-Loop-Helix (bHLH) subgroup Ia genes, SPCH, MUTE and FAMA, mediate sequential steps of stomatal development, and their functions may be conserved in land plants. However, the evolutionary history of the putative SPCH/MUTE/FAMA genes is still greatly controversial, especially the phylogenetic positions of the bHLH Ia members from basal land plants. To better understand the evolutionary pattern and functional diversity of the bHLH genes involved in stomatal development, we made a comprehensive evolutionary analysis of the homologous genes from 54 species representing the major lineages of green plants. The phylogenetic analysis indicated: (1) All bHLH Ia genes from the two basal land plants Physcomitrella and Selaginella were closely related to the FAMA genes of seed plants; and (2) the gymnosperm 'SPCH' genes were sister to a clade comprising the angiosperm SPCH and MUTE genes, while the FAMA genes of gymnosperms and angiosperms had a sister relationship. The revealed phylogenetic relationships are also supported by the distribution of gene structures and previous functional studies. Therefore, we deduce that the function of FAMA might be ancestral in the bHLH Ia subgroup. In addition, the gymnosperm "SPCH" genes may represent an ancestral state and have a dual function of SPCH and MUTE, two genes that could have originated from a duplication event in the common ancestor of angiosperms. Moreover, in angiosperms, SPCHs have experienced more duplications and harbor more copies than MUTEs and FAMAs, which, together with variation of the stomatal development in the entry division, implies that SPCH might have contributed greatly to the diversity of stomatal development. Based on the above, we proposed a model for the correlation between the evolution of stomatal development and the genes involved in this developmental process in land plants.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Bryopsida / genetics*
  • Bryopsida / growth & development
  • Evolution, Molecular*
  • Genes, Plant / physiology*
  • Models, Genetic
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plant Stomata / genetics*
  • Plant Stomata / growth & development
  • Selaginellaceae / genetics*
  • Selaginellaceae / growth & development

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Plant Proteins

Grant support

This work was supported by the National Natural Science Foundation of China (Grant numbers 30870166, 30990240 and 30425028). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.