Mechanisms of stomatal development: an evolutionary view. Evodevo 3:11

Department of Biology, Stanford University, Stanford, CA, 94305-5020, USA. .
EvoDevo (Impact Factor: 3.1). 06/2012; 3(1):11. DOI: 10.1186/2041-9139-3-11
Source: PubMed

ABSTRACT 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.
    The Plant Cell 07/2015; DOI:10.1105/tpc.15.00006 · 9.58 Impact Factor
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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.
    Development 02/2014; 141(6). DOI:10.1242/dev.103531 · 6.27 Impact Factor
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    • "This is not to say that water limitations are unimportant. On the contrary, fluctuations in plant-available water are ubiquitous in the vast majority of terrestrial environments, key to community structure and a major engine of terrestrial plant diversification (Beerling & Woodward 1997; Vaten & Bergmann 2012). In the following pages, we review mechanisms and population dynamic consequences of niche differentiation involving the use of water, and examine the hypothesis that, on a fundamental level, they correspond to temporal niches, stabilized through typically high variability in precipitation. "
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    ABSTRACT: 1. We review plant competition in water-limited environments with focus on temporal niche dynamics and examine implications for diversity—productivity relationships and the response of ecosystem productivity to changes in water availability. The main theses under examination are that (i) plant functional types (PFTs) have distinct resource pulse use and coexist through mechanism of temporal resource use complementarity; and (ii) species of same PFT (functionally redundant species) coexist through distinct recruitment niches. 2. In water-limited systems, opportunities for plant resource uptake and growth fluctuate through time, dependent on precipitation patterns. Species differ in the sensitivities of germination, seedling mortality and adult productivity to pulses of water availability, and this generates opportunity for temporal niche diversification. We illustrate this in two case studies. 3. Case study I. Savannas: This is an example of niche separation between two distinct plant functional types (PFTs), trees and grasses. Several models suggest that the two PFTs have complementary resource pulse use, which regulates their abundances, but other models suggest that tree abundance is regulated by the narrow recruitment niche of trees. Overly restrictive recruitment niches can cause a mismatch between resource availability, PFT composition and ecosystem productivity. 4. Case study II. The tropical dry forest: Here, we examine niche separation between closely related species of same PFT. These species commonly have distinct temporal recruitment niches based on differences in seed and seedling traits. A diversification of recruitment niches may be necessary for sympatric speciation and has the effect of broadening of the recruitment 'portfolio' of a phylogenetic lineage and PFT. 5. Synthesis: Functional diversity, characterized by differences in adult resource use, optimizes ecosystem function in a pulsed resource environment only if PFT abundances are regulated by adult resource use. Regulation through recruitment niches tends to uncouple plant productivity from resource availability. However, we hypothesize that a diversification of recruitment niches within PFTs may help alleviate recruitment limitations and help communities attain a PFT composition that optimizes resource use and permits adaptation to climate change.
    Functional Ecology 08/2013; 27(4):886-897. DOI:10.2307/23480997 · 4.86 Impact Factor
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