Mechanisms of stomatal development: An evolutionary view

Department of Biology, Stanford University, Stanford, CA, 94305-5020, USA. .
EvoDevo (Impact Factor: 3.03). 06/2012; 3(1):11. DOI: 10.1186/2041-9139-3-11
Source: PubMed


Plant development has a significant postembryonic phase that is guided heavily by interactions between the plant and the outside environment. This interplay is particularly evident in the development, pattern and function of stomata, epidermal pores on the aerial surfaces of land plants. Stomata have been found in fossils dating from more than 400 million years ago. Strikingly, the morphology of the individual stomatal complex is largely unchanged, but the sizes, numbers and arrangements of stomata and their surrounding cells have diversified tremendously. In many plants, stomata arise from specialized and transient stem-cell like compartments on the leaf. Studies in the flowering plant Arabidopsis thaliana have established a basic molecular framework for the acquisition of cell fate and generation of cell polarity in these compartments, as well as describing some of the key signals and receptors required to produce stomata in organized patterns and in environmentally optimized numbers. Here we present parallel analyses of stomatal developmental pathways at morphological and molecular levels and describe the innovations made by particular clades of plants.

    • "In grasses , no self - renewing cells are produced in the stomatal lineage ( Liu et al . , 2009 ; Vatén and Bergmann , 2012 ) . The absence of the PPD2 - KIX8 / 9 complex in grasses might therefore reflect the absence of meristemoid amplifying divisions observed in leaves having a two - dimensional growth . "
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    ABSTRACT: Cell number is an important determinant of final organ size. In the leaf, a large proportion of cells are derived from the stomatal lineage. Meristemoids, which are stem cell-like precursor cells, undergo asymmetric divisions, generating several pavement cells adjacent to the two guard cells. However, the mechanism controlling the asymmetric divisions of these stem cells prior to differentiation is not well understood. Here, we characterized PEAPOD (PPD) proteins, the only transcriptional regulators known to negatively regulate meristemoid division. PPD proteins interact with KIX8 and KIX9, which act as adaptor proteins for the corepressor TOPLESS. D3-type cyclin encoding genes were identified among direct targets of PPD2, being negatively regulated by PPDs and KIX8/9. Accordingly, kix8 kix9 mutants phenocopied PPD loss-of-function producing larger leaves resulting from increased meristemoid amplifying divisions. The identified conserved complex might be specific for leaf growth in the second dimension, since it is not present in Poaceae (grasses), which also lack the developmental program it controls. © 2015 American Society of Plant Biologists. All rights reserved.
    No preview · Article · Jul 2015 · The Plant Cell
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    • "Although ZOU possesses a unique C-terminal domain, recent phylogenetic analyses have placed it in bHLH class Ib1, relatively close to the class Ia SPEECHLESS, MUTE and FAMA proteins (Pires and Dolan, 2010). In contrast to ZOU, which is not clearly conserved in bryophytes (Yang et al., 2008), genes encoding both ICE1-like class IIIb and class Ia bHLH proteins can clearly be distinguished in the bryophyte Physcomitrella, which, like angiosperms, produces true stomata in the epidermal cell layer of the sporophyte (Vatén and Bergmann, 2012), leading to the suggestion that the class Ia/IIIb partnership might be ancient, possibly coinciding with the rise of the bryophytes and potentially contributing to the elaboration of true stomata (MacAlister and Bergmann, 2011; Vatén and Bergmann, 2012; Vatén and Bergmann, 2013). ZOU expression in Arabidopsis is strictly limited to the endosperm, which in angiosperms is thought to be the sexualized homolog of the megagametophyte in lower land plants. "
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    ABSTRACT: In Arabidopsis seeds, embryo growth is coordinated with endosperm breakdown. Mutants in the endosperm-specific gene ZHOUPI (ZOU), which encodes a unique basic helix-loop-helix (bHLH) transcription factor, have an abnormal endosperm that persists throughout seed development, significantly impeding embryo growth. Here we show that loss of function of the bHLH-encoding gene INDUCER OF CBP EXPRESSION 1 (ICE1) causes an identical endosperm persistence phenotype. We show that ZOU and ICE1 are co-expressed in the endosperm and interact in yeast via their bHLH domains. We show both genetically and in a heterologous plant system that, despite the fact that both ZOU and ICE1 can form homodimers in yeast, their role in endosperm breakdown requires their heterodimerization. Consistent with this conclusion, we confirm that ZOU and ICE1 regulate the expression of common target genes in the developing endosperm. Finally, we show that heterodimerization of ZOU and ICE1 is likely to be necessary for their binding to specific targets, rather than for their nuclear localization in the endosperm. By comparing our results with paradigms of bHLH function and evolution in animal systems we propose that the ZOU/ICE1 complex might have ancient origins, acquiring novel megagametophyte-specific functions in heterosporous land plants that were conserved in the angiosperm endosperm.
    Full-text · Article · Feb 2014 · Development
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    • "PpSMF1 can also partially complement mute and fama mutants in A. thaliana [31]. In addition, the partnership between the subgroup Ia SPCH/MUTE/FAMA and the subgroup IIIb SCRM/SCRM2 might have an ancient origin, because both of these two subgroups occur in the basal land plant, P. patens [32]. "
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    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.
    Full-text · Article · Nov 2013 · PLoS ONE
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