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AGAMOUS mediates timing of guard cell formation during gynoecium development [1]

['Ailbhe J. Brazel', 'Department Of Biology', 'Maynooth University', 'The Max Plank Institute For Plant Breeding Research', 'Cologne', 'Róisín Fattorini', 'Department Of Biochemistry', 'Systems Biology', 'The University Of Liverpool', 'United Kingdom']

Date: 2023-11

In Arabidopsis thaliana, stomata are composed of two guard cells that control the aperture of a central pore to facilitate gas exchange between the plant and its environment, which is particularly important during photosynthesis. Although leaves are the primary photosynthetic organs of flowering plants, floral organs are also photosynthetically active. In the Brassicaceae, evidence suggests that silique photosynthesis is important for optimal seed oil content. A group of transcription factors containing MADS DNA binding domains is necessary and sufficient to confer floral organ identity. Elegant models, such as the ABCE model of flower development and the floral quartet model, have been instrumental in describing the molecular mechanisms by which these floral organ identity proteins govern flower development. However, we lack a complete understanding of how the floral organ identity genes interact with the underlying leaf development program. Here, we show that the MADS domain transcription factor AGAMOUS (AG) represses stomatal development on the gynoecial valves, so that maturation of stomatal complexes coincides with fertilization. We present evidence that this regulation by AG is mediated by direct transcriptional repression of a master regulator of the stomatal lineage, MUTE, and show data that suggests this interaction is conserved among several members of the Brassicaceae. This work extends our understanding of the mechanisms underlying floral organ formation and provides a framework to decipher the mechanisms that control floral organ photosynthesis.

Photosynthesis supports the growth and development of plants and is mainly associated with leaves. However, other organs, including floral organs, are photosynthetic and contribute to the energy requirements of the plant, which has attracted the interest of crop breeders. Despite its importance, very little is known about the establishment and molecular regulation of floral organ photosynthesis. Here, we describe the developmental progression and regulation of stomatal formation on the female reproductive organs of Arabidopsis thaliana before and after fertilization. Stomata control gas exchange between the plant and the environment, which facilitates photosynthesis and transpiration. We show that stomatal formation coincides with fertilization of the flower but does not depend upon it. Instead, the activity of a master regulator of stomatal development is directly controlled by a flower-specific factor. We present evidence that this regulation is conserved in several members of the mustard plant family (Brassicaceae) and suggest that the timing of stomatal formation on the female reproductive organs may be modified between species, which may have adaptive benefits. Given that floral organs are derived from leaves, this work also broadens and deepens our understanding of how the underlying leaf developmental program is rewired during flower development.

Funding: DSOM was supported by a Humboldt Postdoctoral Fellowship (including stipend), a BBSRC David Phillips Fellowship including salary (BB/T009462/1) and the lab of DSOM was funded by a BBSRC David Phillips Fellowship (BB/T009462/1). AJB is funded by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No 897783, which includes a salary. JM was funded by a BBSRC doctoral training partnership that includes a stipend. GC was funded by the Max Planck Society, a grant from the Deutsche forschungsgemeinschaft ( https://www.dfg.de/ , CO 318/11-1), a grant from the ERC ( https://erc.europa.eu/ , N°339113 – HyLife) and is a member of a DFG-funded Cluster of Excellence ( https://www.dfg.de/ , EXC 2048/1 Project ID: 390686111). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability: All data presented in the manuscript is freely available in figures and tables, and relevant open access databases are cited including ChIP-Hub ( https://biobigdata.nju.edu.cn/ChIPHub/ ). The AG ChIP-Seq data (GSE45938) and the SEP3 ChIP-Seq data (GSE46986) are available at https://www.ncbi.nlm.nih.gov . The seq-DAP-seq data for AG-SEP3 ( https://genome.ucsc.edu/s/ArnaudStigliani/MADS ), Bioproject PRJNA549137 (available at https://www.ncbi.nlm.nih.gov ), and GEO Dataset GSE64581 (available at https://www.ncbi.nlm.nih.gov ).

Here, we investigated the developmental progression and molecular regulation of stomatal development on gynoecial and silique valves in A. thaliana. We describe the normal progression of stomatal development before and after fertilization, and present evidence that AG suppresses this process in A. thaliana and other members of the Brassicaceae. The data presented provide further evidence and mechanism that transcription factors conferring floral organ identity directly suppress aspects of leaf development during floral organ formation. They also provide a framework with which to understand the establishment of the silique as a photosynthetic organ in the Brassicaceae.

The MADS-domain protein AGAMOUS (AG) controls the specification of stamens and carpels and is required for floral meristem termination [ 27 ]. AG interacts with E-class proteins, SEPALLATA 1–4 (SEP1-4), in heterodimeric or tetrameric complexes to coordinate carpel specification and floral meristem termination, with SEP3 playing an especially important role [ 29 , 34 , 39 ]. AG activity promotes carpel development in a partially redundant manner with its closest related paralogs SHATTERPROOF1 (SHP1) and SHP2 [ 40 ]. AG and the SHP proteins also suppress the formation of epidermal hairs (trichomes) during carpel differentiation, which represents the first tangible example of how the floral organ identity proteins modify the underlying leaf development program to generate floral organs [ 35 , 41 ].

Floral organ identity is controlled by a group of transcription factors that contain MADS DNA-binding domains [ 24 – 28 ]. In the absence of their activities, floral organs are converted into leaf-like organs while ectopic expression of these transcription factors is sufficient to transform leaves into floral organs [ 28 – 32 ]. These observations confirmed a long-standing hypothesis that floral organs are derived from leaves [ 33 ]. They also formed the basis of the ABCE model of flower development and the floral quartet model, which largely address organ specification [ 28 – 32 , 34 ]. However, these MADS domain transcription factors continue to be expressed after the floral organs have been specified and they are known to control the expression of genes required for differentiation [ 35 – 38 ]. Identifying the repertoire of differentiation processes that the floral organ identity genes control remains a key challenge [ 25 ].

On leaves of A. thaliana, the stomatal cell lineage is initiated by the asymmetric cell division of a protodermal cell (or meristemoid mother cell), which is regulated by the basic helix-loop-helix (bHLH) transcription factor SPEECHLESS (SPCH) [ 13 – 15 ] ( S1B Fig ). This asymmetric division produces a meristemoid and a stomatal lineage ground cell (SLGC). The meristemoid may then undergo further asymmetric cell divisions to renew itself and produce more SLGCs. Alternatively, a meristemoid may transition into a rounded cell termed a guard mother cell (GMC) [ 14 , 15 ]. The transition from meristemoid to GMC is coordinated by another bHLH transcription factor, MUTE, which also functions to attenuate asymmetric cell divisions [ 16 ]. GMCs then divide symmetrically to produce two guards cells and ultimately a mature stomatal complex, a process that is mediated by a third bHLH transcription factor, FAMA [ 17 ]. Two other bHLH transcription factors, SCREAM (SCRM) and SCRM2, form heterodimers with SPCH, MUTE, and FAMA to coordinate gene expression [ 18 ]. These division steps are regulated such that stomatal complexes are separated by at least one cell, which ensures control of the central pore aperture [ 14 , 15 ]. Several transmembrane receptors have been implicated in this stomatal patterning, such as TOO MANY MOUTHS (TMM), ERECTA (ER), ER-LIKE1 (ERL1), and ERL2 [ 15 , 19 , 20 ]. The activities of these receptors are modulated by the EPIDERMAL PATTERNING FACTORs (EPFs) and EPF-LIKES (EPFLs) secreted peptide families ( S1B Fig ) [ 15 , 21 – 23 ].

In eudicots, such as Arabidopsis thaliana, flowers are composed of four types of floral organs: sepals, petals, stamens, and carpels. The sepals contain high levels of chlorophyll and bear stomata, making them leaf-like in appearance. In contrast, mature petals and stamens lack substantial concentrations of chlorophyll [ 1 , 2 ]. Stomata are absent from petals but modified stomata are present on the abaxial surfaces of anthers [ 1 , 3 ]. In A. thaliana, the ovules are encased within the gynoecium which is formed of two fused carpels and other tissues that arise from the carpels, such as the style, stigma and replum [ 1 , 4 ] ( S1A Fig ). Although the gynoecial valves lack stomata, they are present on the differentiated and elongated silique valve epidermis [ 5 , 6 ]. Stomata on siliques enable atmospheric carbon fixation to support photosynthesis, and photosynthetic activity of siliques has been demonstrated in several members of the Brassicaceae family including A. thaliana [ 7 – 10 ]. This photosynthetic activity positively influences seed oil content and is of interest to crop breeders [ 8 , 9 , 11 ]. Stomata also support transpiration, which drives the movement of nutrients through the plant and simultaneously facilitates cooling [ 12 ]. However, very little is known about the molecular mechanisms of stomatal development on these organs.

Results

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[1] Url: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1011000

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