Summary
Stomata are cellular breathing pores on leaves that open and close to absorb photosynthetic carbon dioxide and to restrict water loss through transpiration, respectively. Grasses (Poaceae) ...form morphologically innovative stomata, which consist of two dumbbell‐shaped guard cells flanked by two lateral subsidiary cells (SCs). This ‘graminoid’ morphology is associated with faster stomatal movements leading to more water‐efficient gas exchange in changing environments. Here, we offer a genetic and mechanistic perspective on the unique graminoid form of grass stomata and the developmental innovations during stomatal cell lineage initiation, recruitment of SCs and stomatal morphogenesis. Furthermore, the functional consequences of the four‐celled, graminoid stomatal morphology are summarized. We compile the identified players relevant for stomatal opening and closing in grasses, and discuss possible mechanisms leading to cell‐type‐specific regulation of osmotic potential and turgor. In conclusion, we propose that the investigation of functionally superior grass stomata might reveal routes to improve water‐stress resilience of agriculturally relevant plants in a changing climate.
Significance Statement
A key challenge for plants is to efficiently use water, particularly when growing in a hot and dry climate. Stomata – cellular breathing pores on leaves that mediate gas exchange between plant and atmosphere – have a pivotal role in controlling water‐use efficiency. Stomata can adjust their pore size to balance carbon dioxide uptake with water vapour loss. Interestingly, grasses like the three most important food crops rice, maize and wheat have improved stomata that can regulate water use more efficiently by opening and closing faster than other plants. Rapid stomatal movements are linked to the grass stomata's unique morphology consisting of dumbbell‐shaped guard cells and lateral subsidiary or helper cells. Recently, work on domesticated and wild grass species has started to reveal some of the secrets regarding how grass stomata form and function more efficiently.
Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner and is regulated by the differential epigenetic marking of the parental alleles. In plants, genomic ...imprinting has been primarily described for genes expressed in the endosperm, a tissue nourishing the developing embryo that does not contribute to the next generation. In Arabidopsis, the genes MEDEA (MEA) and PHERES1 (PHE1), which are imprinted in the endosperm, are also expressed in the embryo; whether their embryonic expression is regulated by imprinting or not, however, remains controversial. In contrast, the maternally expressed in embryo 1 (mee1) gene of maize is clearly imprinted in the embryo. We identified several imprinted candidate genes in an allele-specific transcriptome of hybrid Arabidopsis embryos and confirmed parent-of-origin-dependent, monoallelic expression for eleven maternally expressed genes (MEGs) and one paternally expressed gene (PEG) in the embryo, using allele-specific expression analyses and reporter gene assays. Genetic studies indicate that the Polycomb Repressive Complex 2 (PRC2) but not the DNA METHYLTRANSFERASE1 (MET1) is involved in regulating imprinted expression in the embryo. In the seedling, all embryonic MEGs and the PEG are expressed from both parents, suggesting that the imprint is erased during late embryogenesis or early vegetative development. Our finding that several genes are regulated by genomic imprinting in the Arabidopsis embryo clearly demonstrates that this epigenetic phenomenon is not a unique feature of the endosperm in both monocots and dicots.
Stomata, epidermal valves facilitating plant–atmosphere gas exchange, represent a powerful model for understanding cell fate and pattern in plants. Core basic helix–loop–helix (bHLH) transcription ...factors regulating stomatal development were identified in Arabidopsis, but this dicot’s developmental pattern and stomatal morphology represent only one of many possibilities in nature. Here, using unbiased forward genetic screens, followed by analysis of reporters and engineered mutants, we show that stomatal initiation in the grass Brachypodium distachyon uses orthologs of stomatal regulators known from Arabidopsis but that the function and behavior of individual genes, the relationships among genes, and the regulation of their protein products have diverged. Our results highlight ways in which a kernel of conserved genes may be alternatively wired to produce diversity in patterning and morphology and suggest that the stomatal transcription factor module is a prime target for breeding or genome modification to improve plant productivity.
Defining the contributions and interactions of paternal and maternal genomes during embryo development is critical to understand the fundamental processes involved in hybrid vigor, hybrid sterility, ...and reproductive isolation. To determine the parental contributions and their regulation during
Arabidopsis embryogenesis, we combined deep-sequencing-based RNA profiling and genetic analyses. At the 2–4 cell stage there is a strong, genome-wide dominance of maternal transcripts, although transcripts are contributed by both parental genomes. At the globular stage the relative paternal contribution is higher, largely due to a gradual activation of the paternal genome. We identified two antagonistic maternal pathways that control these parental contributions. Paternal alleles are initially downregulated by the chromatin siRNA pathway, linked to DNA and histone methylation, whereas transcriptional activation requires maternal activity of the histone chaperone complex CAF1. Our results define maternal epigenetic pathways controlling the parental contributions in plant embryos, which are distinct from those regulating genomic imprinting.
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► The early
Arabidopsis embryonic transcriptome has a dominant maternal contribution ► The paternal contribution increases gradually during early embryogenesis ► Parental contributions are maternally controlled by the chromatin siRNA pathway ► Paternal activation requires maternal activity of histone chaperone complex CAF1
Plants optimize carbon assimilation while limiting water loss by adjusting stomatal aperture. In grasses, a developmental innovation—the addition of subsidiary cells (SCs) flanking two ...dumbbell-shaped guard cells (GCs)—is linked to improved stomatal physiology. Here, we identify a transcription factor necessary and sufficient for SC formation in the wheat relative Brachypodium distachyon. Unexpectedly, the transcription factor is an ortholog of the stomatal regulator AtMUTE, which defines GC precursor fate in Arabidopsis. The novel role of BdMUTE in specifying lateral SCs appears linked to its acquisition of cell-to-cell mobility in Brachypodium. Physiological analyses on SC-less plants experimentally support classic hypotheses that SCs permit greater stomatal responsiveness and larger range of pore apertures. Manipulation of SC formation and function in crops, therefore, may be an effective approach to enhance plant performance.
Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner. It is achieved by the differential epigenetic marking of parental alleles. Over the past decade, ...studies in the model systems Arabidopsis thaliana and maize (Zea mays) have shown a strong correlation between silent or active states with epigenetic marks, such as DNA methylation and histone modifications, but the nature of the primary imprint has not been clearly established for all imprinted genes. Phenotypes and expression patterns of imprinted genes have fueled the perception that genomic imprinting is specific to the endosperm, a seed tissue that does not contribute to the next generation. However, several lines of evidence suggest a potential role for imprinting in the embryo, raising questions as to how imprints are erased and reset from one generation to the next. Imprinting regulation in flowering plants shows striking similarities, but also some important differences, compared with the mechanisms of imprinting described in mammals. For example, some imprinted genes are involved in seed growth and viability in plants, which is similar in mammals, where imprinted gene regulation is essential for embryonic development. However, it seems to be more flexible in plants, as imprinting requirements can be bypassed to allow the development of clonal offspring in apomicts.
Genomic imprinting leads to different expression levels of maternally and paternally derived alleles. Over the last years, major progress has been made in identifying novel imprinted candidate genes ...in plants, owing to affordable next-generation sequencing technologies. However, reports on sequencing the transcriptome of hybrid F1 seed tissues strongly disagree about how many and which genes are imprinted. This raises questions about the relative impact of biological, environmental, technical, and analytic differences or biases. Here, we adopt a statistical approach, frequently used in RNA-seq data analysis, which properly models count overdispersion and considers replicate information of reciprocal crosses. We show that our statistical pipeline outperforms other methods in identifying imprinted genes in simulated and real data. Accordingly, reanalysis of genome-wide imprinting studies in Arabidopsis and maize shows that, at least for Arabidopsis, an increased agreement across datasets could be observed. For maize, however, consistent reanalysis did not yield a larger overlap between the datasets. This suggests that the discrepancy across publications might be partially due to different analysis pipelines but that technical, biological, and environmental factors underlie much of the discrepancy between datasets. Finally, we show that the set of genes that can be characterized regarding allelic bias by all studies with minimal confidence is small (~8,000/27,416 genes for Arabidopsis and ~12,000/39,469 for maize). In conclusion, we propose to use biologically replicated reciprocal crosses, high sequence coverage, and a generalized linear model approach to identify differentially expressed alleles in developing seeds.
Grass stomata recruit lateral subsidiary cells (SCs), which are key to the unique stomatal morphology and the efficient plant-atmosphere gas exchange in grasses. Subsidiary mother cells (SMCs) ...strongly polarise before an asymmetric division forms a SC. Yet apart from a proximal polarity module that includes PANGLOSS1 (PAN1) and guides nuclear migration, little is known regarding the developmental processes that form SCs. Here, we used comparative transcriptomics of developing wild-type and SC-less
leaves in the genetic model grass
to identify novel factors involved in SC formation. This approach revealed BdPOLAR, which forms a novel, distal polarity domain in SMCs that is opposite to the proximal PAN1 domain. Both polarity domains are required for the formative SC division yet exhibit various roles in guiding pre-mitotic nuclear migration and SMC division plane orientation, respectively. Nonetheless, the domains are linked as the proximal domain controls polarisation of the distal domain. In summary, we identified two opposing polarity domains that coordinate the SC division, a process crucial for grass stomatal physiology.
Plants and animals reproduce sexually via specialized, highly differentiated gametes. Yet, gamete formation drastically differs between the two kingdoms. In flowering plants, the specification of ...cells destined to enter meiosis occurs late in development, gametic and accessory cells are usually derived from the same meiotic product, and two distinct female gametes involved in double fertilization differentiate. This poses fascinating questions in terms of gamete development and the associated epigenetic processes. Although studies in this area remain at their infancy, it becomes clear that large-scale epigenetic reprograming, involving RNA-directed DNA methylation, chromatin modifications, and nucleosome remodeling, contributes to the establishment of transcriptionally repressive or permissive epigenetic landscapes. Furthermore, a role for small RNAs in the regulation of transposable elements during gametogenesis is emerging.
Summary
Stomata are breathing pores on leaves that balance photosynthetic carbon dioxide uptake and water vapor loss. Stomatal morphology and complexity are rather diverse when considering stomatal ...subsidiary cells (SCs). Subsidiary cells are adjacent to the central guard cells (GCs) and are morphologically distinct from other epidermal cells. Yet, how various SCs develop and whether and how they support stomatal gas exchange physiology outside of the grass family is largely unknown. Here, we discuss the development, ontogeny, and putative function of paracytic vs anisocytic SCs, which can be found in grasses and Crassulaceae succulents, respectively. First, we highlight recent advances in understanding how grasses form stomatal SCs. We then summarize novel insights into stomatal development in SC‐less Arabidopsis to speculate on how this stomatal program might be rewired to enable anisocytic SC formation. Finally, we discuss the functional relevance of paracytic SCs in grasses and the putative roles of anisocytic SCs in succulents.
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