Stomatal development in the grasses McKown, Katelyn H.; Bergmann, Dominique C.
The New phytologist,
September 2020, Letnik:
227, Številka:
6
Journal Article
Recenzirano
Odprti dostop
When plants emerged from their aquatic origins to colonise land, they needed to avoid desiccation while still enabling gas and water exchange with the environment. The solution was the development of ...a waxy cuticle interrupted by epidermal pores, known as stomata. Despite the importance of stomata in plant physiology and their contribution to global water and carbon cycles, our knowledge of the genetic basis of stomatal development is limited mostly to the model dicot, Arabidopsis thaliana. This limitation is particularly troublesome when evaluating grasses, whose members represent our most agriculturally significant crops. Grass stomatal development follows a trajectory strikingly different from Arabidopsis and their uniquely shaped four-celled stomatal complexes are especially responsive to environmental inputs. Thus, understanding the development and regulation of these efficient complexes is of particular interest for the purposes of crop engineering. This review focuses on genetic regulation of grass stomatal development and prospects for the future, highlighting discoveries enabled by parallel comparative investigations in cereal crops and related genetic model species such as Brachypodium distachyon.
Mechanical information is an important contributor to cell polarity in uni- and multicellular systems 1–3. In planar tissues like the Drosophila wing, cell polarity reorients during growth as cells ...divide and reorganize 4. In another planar tissue, the Arabidopsis leaf epidermis 5, polarized, asymmetric divisions of stomatal stem cells (meristemoid mother cells MMCs) are fundamental for the generation and patterning of multiple cell types, including stomata. The activity of key transcription factors, polarizing factors 6, and peptide signals 7 explains some local stomatal patterns emerging from the behavior of a few lineally related cells 6, 8–11. Here we demonstrate that, in addition to locally acting signals, tissue-wide mechanical forces can act as organizing cues, and that they do so by influencing the polarity of individual MMCs. If the mechanical stress environment in the tissue is altered through stretching or cell ablations, cellular polarity changes in response. In turn, polarity predicts the orientation of cellular and tissue outgrowth, leading to increased mechanical conflicts between neighboring cells. This interplay among growth, oriented divisions, and cell specification could contribute to the characteristic patterning of stomatal guard cells in the context of a growing leaf.
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•Markers of stomatal lineage cell polarity respond to local and leaf-wide information•Polarized protein localization predicts cellular outgrowth direction•Mechanical conflicts between neighboring cells can orient individual cell polarities•Chemical signaling overrules mechanics to dictate cellular polarity orientation
Polarized tissues are themselves often made of polarized cells. Bringmann and Bergmann show that, in the leaf epidermis, orientation of cortical polarity proteins is guided by mechanical information derived from growth dynamics of the leaf. In turn, polarity proteins anticipate cell outgrowth, thus feeding back on overall tissue development.
The plant stomatal lineage manifests features common to many developmental contexts: precursor cells are chosen from an initially equivalent field of cells, undergo asymmetric and self-renewing ...divisions, communicate among themselves and respond to information from a distance. As we review here, the experimental accessibility of these epidermal lineages, particularly in Arabidopsis, has made stomata a conceptual and technical framework for the study of cell fate, stem cells, and cell polarity in plants.
Stomata are structures on the surfaces of most land plants that are required for gas exchange between plants and their environment. In
, stomata comprise two kidney bean-shaped epidermal guard cells ...that flank a central pore overlying a cavity in the mesophyll. These guard cells can adjust their shape to occlude or facilitate access to this pore, and in so doing regulate the release of water vapor and oxygen from the plant, in exchange for the intake of carbon dioxide from the atmosphere. Stomatal guard cells are the end product of a specialized lineage whose cell divisions and fate transitions ensure both the production and pattern of cells in aerial epidermal tissues. The stomatal lineage is dynamic and flexible, altering stomatal production in response to environmental change. As such, the stomatal lineage is an excellent system to study how flexible developmental transitions are regulated in plants. In this Cell Science at a Glance article and accompanying poster, we will summarize current knowledge of the divisions and fate decisions during stomatal development, discussing the role of transcriptional regulators, cell-cell signaling and polarity proteins. We will highlight recent work that links the core regulators to systemic or environmental information and provide an evolutionary perspective on stomata lineage regulators in plants.
Multicellular development depends on generating and precisely positioning distinct cell types within tissues. During leaf development, pores in the epidermis called stomata are spaced at least one ...cell apart for optimal gas exchange. This pattern is primarily driven by iterative asymmetric cell divisions (ACDs) in stomatal progenitors, which generate most of the cells in the tissue. A plasma membrane-associated polarity crescent defined by BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) and BREVIS RADIX family (BRXf) proteins is required for asymmetric divisions and proper stomatal pattern, but the cellular mechanisms that orient ACDs remain unclear. Here, utilizing long-term, quantitative time-lapse microscopy, we identified two oppositely oriented nuclear migrations that precede and succeed ACD during epidermal patterning. The pre- and post-division migrations are dependent on microtubules and actin, respectively, and the polarity crescent is the unifying landmark that is both necessary and sufficient to orient both nuclear migrations. We identified a specific and essential role for MYOXI-I in controlling post-ACD nuclear migration. Loss of MYOXI-I decreases stomatal density, owing to an inability to accurately orient a specific subset of ACDs. Taken together, our analyses revealed successive and polarity-driven nuclear migrations that regulate ACD orientation in the Arabidopsis stomatal lineage.
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•Nuclear migrations flank asymmetric divisions in the Arabidopsis stomatal lineage•A BASL/BRXf polarity crescent orients both nuclear migrations•MYOXI-I is required for nuclear migration after asymmetric division•Loss of directed nuclear migrations correlates with division orientation defects
How are asymmetric divisions oriented in developing plant tissues? Muroyama et al. find that oppositely oriented nuclear migrations flank asymmetric divisions in the Arabidopsis stomatal lineage. Despite having distinct cytoskeletal requirements, both migrations use BASL as a spatial landmark and are collectively required for division orientation.
Cellular processes rely on the intimate interplay of different molecules, including DNA, RNA, proteins, and metabolites. Obtaining and integrating data on their abundance and dynamics at high ...temporal and spatial resolution are essential for our understanding of plant growth and development. In the past decade, enzymatic proximity labeling (PL) has emerged as a powerful tool to study local protein and nucleotide ensembles, discover protein-protein and protein-nucleotide interactions, and resolve questions about protein localization and membrane topology. An ever-growing number and continuous improvement of enzymes and methods keep broadening the spectrum of possible applications for PL and make it more accessible to different organisms, including plants. While initial PL experiments in plants required high expression levels and long labeling times, recently developed faster enzymes now enable PL of proteins on a cell type-specific level, even with low-abundant baits, and in different plant species. Moreover, expanding the use of PL for additional purposes, such as identification of locus-specific gene regulators or high-resolution electron microscopy may now be in reach. In this review, we give an overview of currently available PL enzymes and their applications in mammalian cell culture and plants. We discuss the challenges and limitations of PL methods and highlight open questions and possible future directions for PL in plants.
Plants must coordinate the regulation of biochemistry and anatomy to optimize photosynthesis and water-use efficiency. The formation of stomata, epidermal pores that facilitate gas exchange, is ...highly coordinated with other aspects of photosynthetic development. The signalling pathways controlling stomata development are not fully understood, although mitogen-activated protein kinase (MAPK) signalling is known to have key roles. Here we demonstrate in Arabidopsis that brassinosteroid regulates stomatal development by activating the MAPK kinase kinase (MAPKKK) YDA (also known as YODA). Genetic analyses indicate that receptor kinase-mediated brassinosteroid signalling inhibits stomatal development through the glycogen synthase kinase 3 (GSK3)-like kinase BIN2, and BIN2 acts upstream of YDA but downstream of the ERECTA family of receptor kinases. Complementary in vitro and in vivo assays show that BIN2 phosphorylates YDA to inhibit YDA phosphorylation of its substrate MKK4, and that activities of downstream MAPKs are reduced in brassinosteroid-deficient mutants but increased by treatment with either brassinosteroid or GSK3-kinase inhibitor. Our results indicate that brassinosteroid inhibits stomatal development by alleviating GSK3-mediated inhibition of this MAPK module, providing two key links; that of a plant MAPKKK to its upstream regulators and of brassinosteroid to a specific developmental output.
Plant cells maintain remarkable developmental plasticity, allowing them to clonally reproduce and to repair tissues following wounding; yet plant cells normally stably maintain consistent identities. ...Although this capacity was recognized long ago, our mechanistic understanding of the establishment, maintenance, and erasure of cellular identities in plants remains limited. Here, we develop a cell-type–specific reprogramming system that can be probed at the genome-wide scale for alterations in gene expression and histone modifications. We show that relationships among H3K27me3, H3K4me3, and gene expression in single cell types mirror trends from complex tissue, and that H3K27me3 dynamics regulate guard cell identity. Further, upon initiation of reprogramming, guard cells induce H3K27me3-mediated repression of a regulator of wound-induced callus formation, suggesting that cells in intact tissues may have mechanisms to sense and resist inappropriate dedifferentiation. The matched ChIP-sequencing (seq) and RNA-seq datasets created for this analysis also serve as a resource enabling inquiries into the dynamic and global-scale distribution of histone modifications in single cell types in plants.
Dynamic cell identities underlie flexible developmental programs. The stomatal lineage in the Arabidopsis leaf epidermis features asynchronous and indeterminate divisions that can be modulated by ...environmental cues. The products of the lineage, stomatal guard cells and pavement cells, regulate plant-atmosphere exchanges, and the epidermis as a whole influences overall leaf growth. How flexibility is encoded in development of the stomatal lineage and how cell fates are coordinated in the leaf are open questions. Here, by leveraging single-cell transcriptomics and molecular genetics, we uncovered models of cell differentiation within Arabidopsis leaf tissue. Profiles across leaf tissues identified points of regulatory congruence. In the stomatal lineage, single-cell resolution resolved underlying cell heterogeneity within early stages and provided a fine-grained profile of guard cell differentiation. Through integration of genome-scale datasets and spatiotemporally precise functional manipulations, we also identified an extended role for the transcriptional regulator SPEECHLESS in reinforcing cell fate commitment.
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•Distinct models of cell differentiation and lineage trajectories define leaf tissue•Cell-cycle regulators exhibit distinct, yet overlapping, expression profiles•Flexible stomatal lineage cell states exist along a continuum•Single-cell resolution refines cell fate commitment decisions that yield stomata
How do cells build developmentally flexible organs? Lopez-Anido et al. employed single-cell transcriptomics to uncover distinct models of cell differentiation within Arabidopsis leaf tissue. Along with revealing dynamics of cellular programs, they identified underlying cell heterogeneity within the epidermal lineage and interrogated new roles for a core transcriptional regulator.
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