Out of the Mouths of Plants: The Molecular Basis of the Evolution and Diversity of Stomatal Development

Peterson, Kylee M.; Rychel, Amanda L.; Torii, Keiko U.

doi:10.1105/tpc.109.072777

Cited by 151 publications

(122 citation statements)

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“…The meristemoid reiterates several rounds of asymmetric cell divisions, producing neighboring nonstomatal cells (stomatal lineage ground cells [SLGCs]) prior to differentiating into a guard mother cell (GMC). The GMC undergoes a single symmetric division and terminally differentiates into a set of paired guard cells (GCs) that constitute a stoma (Bergmann and Sack, 2007;Peterson et al, 2010) (Figure 1A). …”

Section: Introductionmentioning

confidence: 99%

Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations inArabidopsis

et al. 2011

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The balance between maintenance and differentiation of stem cells is a central question in developmental biology. Development of stomata in Arabidopsis thaliana begins with de novo asymmetric divisions producing meristemoids, proliferating precursor cells with stem cell-like properties. The transient and asynchronous nature of the meristemoid has made it difficult to study its molecular characteristics. Synthetic combination of stomatal differentiation mutants due to loss-or gain-of-function mutations in SPEECHLESS, MUTE, and SCREAM create seedlings with an epidermis overwhelmingly composed of pavement cells, meristemoids, or stomata, respectively. Through transcriptome analysis, we define and characterize the molecular signatures of meristemoids. The reporter localization studies of meristemoid-enriched proteins reveals pathways not previously associated with stomatal development. We identified a novel protein, POLAR, and demonstrate through time-lapse live imaging that it exhibits transient polar localization and segregates unevenly during meristemoid asymmetric divisions. The polar localization of POLAR requires BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE. Comparative bioinformatic analysis of the transcriptional profiles of a meristemoid with shoot and root apical meristems highlighted cytokinin signaling and the ERECTA family receptor-like kinases in the broad regulation of stem cell populations. Our work reveals molecular constituents of stomatal stem cells and illuminates a common theme among stem cell populations in plants.

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Section: Introductionmentioning

confidence: 99%

Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations inArabidopsis

et al. 2011

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“…The presence of epidermal neighboring cells to provide an exchange of osmotic solute also is argued to eliminate the mechanical back pressure from guard cells. Indeed, Franks and Farquhar (2007) have noted the distinct arrangements of stomatal complexes between species and their association with adjacent epidermal cells allowing the ion exchange required for the opening process.The majority of plant species follow a one-cell spacing rule during epidermal development that leads to the separation of stomata by at least one epidermal cell (Geisler et al, 2000;Peterson et al, 2010;Pillitteri and Dong, 2013). However, there are several genera that diverge from this rule.…”

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confidence: 99%

Stomatal Spacing Safeguards Stomatal Dynamics by Facilitating Guard Cell Ion Transport Independent of the Epidermal Solute Reservoir

2016

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Stomata enable gaseous exchange between the interior of the leaf and the atmosphere through the stomatal pore. Control of the pore aperture depends on osmotic solute accumulation by, and its loss from the guard cells surrounding the pore. Stomata in most plants are separated by at least one epidermal cell, and this spacing is thought to enhance stomatal function, although there are several genera that exhibit stomata in clusters. We made use of Arabidopsis (Arabidopsis thaliana) stomatal patterning mutants to explore the impact of clustering on guard cell dynamics, gas exchange, and ion transport of guard cells. These studies showed that stomatal clustering in the Arabidopsis too many mouths (tmm1) mutant suppressed stomatal movements and affected CO 2 assimilation and transpiration differentially between dark and light conditions and were associated with alterations in K + channel gating. These changes were consistent with the impaired dynamics of tmm1 stomata and were accompanied by a reduced accumulation of K + ions in the guard cells. Our findings underline the significance of spacing for stomatal dynamics. While stomatal spacing may be important as a reservoir for K + and other ions to facilitate stomatal movements, the effects on channel gating, and by inference on K + accumulation, cannot be explained on the basis of a reduced number of epidermal cells facilitating ion supply to the guard cells.Stomata are pores found in the epidermis of most aerial parts of plants and are formed between a specialized pair of cells, the guard cells. Stomata facilitate the uptake of CO 2 at the expense of water vapor release via transpiration (Hetherington and Woodward, 2003). Hence, stomata play a crucial role in the physiology of plants. They permit gaseous exchange between the environment and the inside of the leaf for photosynthesis and, in turn, they influence the water use efficiency and growth of the plant. Mathematical models have suggested that historical changes in the freshwater resources can be attributed to stomatal transpiration, and it has been argued that the manipulation of stomata will be an important factor in ensuring water availability over the next 20 to 30 years (UNESCO World Water Development Report, 2015). Efforts to develop crops with higher water use efficiency through conventional breeding strategies have led to some successes, including the Drysdale wheat (Triticum aestivum) variety (Condon et al., 2002). It is likely that further advances will be possible as we gain insights into the physiology of stomata in situ.The regulation of gas exchange is achieved by controlling the stomatal pore. Stomata respond dynamically to environmental changes, including light quality and intensity, ambient CO 2 concentration, and humidity (Aphalo and Jarvis, 1991;Hetherington and Woodward, 2003;Shimazaki et al., 2007). Stomatal movements result from changes in guard cell volume and turgor and are driven by solute and water fluxes across the plasma membrane and tonoplast of guard cells. In particular, fluxes of ...

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“…Indeed, the master regulatory bHLHs are conserved down to non-vascular, basal land plants, such as moss (MacAlister and Bergmann, 2011;Peterson et al, 2010). However, the arrangements of stomata in the epidermis exhibit diversity among taxa (Peterson et al, 2010). It is entirely possible that each plant taxon has adopted unique signaling or polarity components to enforce the one-cell spacing rule.…”

Section: Discussionmentioning

confidence: 99%

“…Owing to their essential physiological functions, the development of stomata is evolutionarily constrained in the land plants. Indeed, the master regulatory bHLHs are conserved down to non-vascular, basal land plants, such as moss (MacAlister and Bergmann, 2011;Peterson et al, 2010). However, the arrangements of stomata in the epidermis exhibit diversity among taxa (Peterson et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…This grass species undergoes a characteristic cell division sequence, giving rise to a stomatal complex with dumbbell-shaped GCs. Instead of asymmetric amplifying divisions of meristemoids, asymmetric divisions of subsidiary mother cells (SMCs), which neighbor GMCs, generate subsidiary cells with specialized functions (Peterson et al, 2010;Stebbins and Shah, 1960). Two Maize LRRRLKs, PANGROSS2 (PAN2) and PAN1, as well a ROP protein, promote the pre-mitotic polarity and subsequent ACD of SMCs.…”

Section: Signal Integration Controlling Upstream Signaling Ligandsmentioning

confidence: 99%

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Lineage-specific stem cells, signals and asymmetries during stomatal development

Han

Torii

2016

Development

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Stomata are dispersed pores found in the epidermis of land plants that facilitate gas exchange for photosynthesis while minimizing water loss. Stomata are formed from progenitor cells, which execute a series of differentiation events and stereotypical cell divisions. The sequential activation of master regulatory basic-helix-loop-helix (bHLH) transcription factors controls the initiation, proliferation and differentiation of stomatal cells. Cell-cell communication mediated by secreted peptides, receptor kinases, and downstream mitogenactivated kinase cascades enforces proper stomatal patterning, and an intrinsic polarity mechanism ensures asymmetric cell divisions. As we review here, recent studies have provided insights into the intrinsic and extrinsic factors that control stomatal development. These findings have also highlighted striking similarities between plants and animals with regards to their mechanisms of specialized cell differentiation.

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Out of the Mouths of Plants: The Molecular Basis of the Evolution and Diversity of Stomatal Development

Cited by 151 publications

References 48 publications

Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations inArabidopsis

Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations inArabidopsis

Stomatal Spacing Safeguards Stomatal Dynamics by Facilitating Guard Cell Ion Transport Independent of the Epidermal Solute Reservoir

Lineage-specific stem cells, signals and asymmetries during stomatal development

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