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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.

Evolution of the bHLH Genes Involved in Stomatal Development: Implications for the Expansion of Developmental Complexity of Stomata in Land Plants