A MAPKK Kinase Gene Regulates Extra-Embryonic Cell Fate in Arabidopsis

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110

Plants, as sessile organisms, must coordinate various physiological processes to adapt to ever-changing surrounding environments. Stomata, the epidermal pores facilitating gas and water exchange, play important roles in optimizing photosynthetic efficiency and adaptability. Stomatal development is under the control of an intrinsic program mediated by a secretory peptide gene familynamely, EPIDERMAL PATTERNING FACTOR, including positively acting STOMAGEN/EPFL9. The phytohormone brassinosteroids and environment factor light also control stomatal production. However, whether auxin regulates stomatal development and whether peptide signaling is coordinated with auxin signaling in the regulation of stomatal development remain largely unknown. Here we show that auxin negatively regulates stomatal development through MONOPTEROS (also known as ARF5) repression of the mobile peptide gene STOMAGEN in mesophyll. Through physiological, genetic, transgenic, biochemical, and molecular analyses, we demonstrate that auxin inhibits stomatal development through the nuclear receptor TIR1/AFB-mediated signaling, and that MONOPTEROS directly binds to the STOMAGEN promoter to suppress its expression in mesophyll and inhibit stomatal development. Our results provide a paradigm of cross-talk between phytohormone auxin and peptide signaling in the regulation of stomatal production.A uxin is the first identified phytohormone, which exerts multifaceted influences on plant growth and development, such as embryonic root initiation (1, 2), shoot apical meristem function (3), and floral primordia initiation (4). As a "molecular glue," auxin facilitates the formation of its coreceptor complexes comprising F-box proteins (TIR1/AFBs) and AUXIN/INDOLE-3-ACETIC ACID proteins (AUX/IAAs), and subsequent AUX/ IAAs ubiquitination and degradation by 26S proteasome, thus releasing auxin response factors (ARFs) from AUX/IAAs repression to regulate auxin-responsive gene expression by either activation or repression (2, 3, 5-11). Although many physiologic processes are reported to be regulated by auxin (1-4, 6, 12), the full understanding of the functions of this versatile phytohormone has not been reached.Stomata, the pores flanked by a pair of guard cells, mainly constitute the epidermis of plant leaves together with trichomes and neighboring pavement cells that separate stomata to maintain the one-cell spacing rule (13,14). As a gas and water passage between external environment and internal plant tissue, stomata play important roles in photosynthesis and global carbon and water circulation (15). Stomatal generation undergoes several stages, including meristemoid mother cell, meristemoid, guard mother cell, and guard cells, which is modulated by an intrinsic program (14) mainly involving putative peptide ligands [EPI-DERMAL PATTERNING FACTOR (EPF) family] (16-20), membrane proteins (receptor-like protein TMM and receptorlike kinase ERECTA family) (21-23), MAPK cascades (protein kinase YDA, MKK4/5/7/9, and MPK3/6) (24-26), and transcription factors (bHLH...

Section: Resultsmentioning

confidence: 99%

Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll

Zhang

et al. 2014

124

110

“…In Col-0 plants, abscission occurs from flower positions 7 to 9. Flowers from stage 15 (13) of 8-week-old Col-0, MKK4-MKK5RNAi, hae hsl2, and MPK6 KR were embedded in Epon-Spurr's resin (22). Thin sections (2.5 m) were obtained with a Leica RM2065 microtome equipped with glass knives and stained with in 0.05% toluidine blue.…”

Section: Histochemical Gusmentioning

confidence: 99%

Regulation of floral organ abscission in Arabidopsis thaliana

Cho

Larue

Chevalier

et al. 2008

313

421

Abscission is a developmental program that results in the active shedding of infected or nonfunctional organs from a plant body. Here, we establish a signaling pathway that controls abscission in Arabidopsis thaliana from ligand, to receptors, to downstream effectors. Loss of function mutations in Inflorescence Deficient in Abscission (IDA), which encodes a predicted secreted small protein, the receptor-like protein kinases HAESA (HAE) and HAESA-like 2 (HSL2), the Mitogen-Activated Protein Kinase Kinase 4 (MKK4) and MKK5, and a dominant-negative form of Mitogen-Activated Protein Kinase 6 (MPK6) in a mpk3 mutant background all have abscission-defective phenotypes. Conversely, expression of constitutively active MKKs rescues the abscission-defective phenotype of hae hsl2 and ida plants. Additionally, in hae hsl2 and ida plants, MAP kinase activity is reduced in the receptacle, the part of the stem that holds the floral organs. Plants overexpressing IDA in a hae hsl2 background have abscission defects, indicating HAE and HSL2 are epistatic to IDA. Taken together, these results suggest that the sequential action of IDA, HAE and HSL2, and a MAP kinase cascade regulates the programmed separation of cells in the abscission zone.protein phosphorylation ͉ signal transduction A bscission is a physiological process that involves the programmed separation of entire organs, such as leaves, petals, flowers, and fruit. Abscission allows plants to discard nonfunctional or infected organs, and promotes dispersion of progeny. At the cellular level, abscission is the hydrolysis of the middle lamella of an anatomically specialized cell layer, the abscission zone (AZ), by cell wall-modifying and hydrolyzing enzymes. Thus, abscission requires both the formation of the AZ early in the development of a plant organ and the subsequent activation of the cell separation response (1-4).Studies using Arabidopsis thaliana have implicated the involvement of several different genes in the control of abscission including potential signal molecules, receptors and other gene products (4). HAESA (HAE), one of the first Arabidopsis receptor-like protein kinases (RLK) identified, is expressed in floral organ AZs and antisense experiments show a reduction in the level of HAE protein is correlated with the degree of defective floral organ abscission. Expression of HAE is not altered in etr1-1 (an ethylene-insensitive mutation), implying an ethyleneindependent role in abscission (5). Inflorescence Deficient in Abscission (IDA) encodes a small protein with an N-terminal signal peptide. Analysis of ida mutant plants indicates IDA regulates floral organ abscission through an ethylene insensitive pathway (6). Overexpression of IDA results in early abscission and the production of a white substance in the floral AZs. The main components of the white substance are arabinose and galactose (7).Here, we report that components of a MAPK signaling cascade also have roles in the regulation of abscission. A MAPK cascade is a regulatory module with three protein kina...

“…The key morphogenetic event in plant embryogenesis is formation of the apicalbasal pattern via establishment of the proliferating embryo proper (apical) and the terminally differentiated suspensor (basal). Developmental programs of the embryo proper and the suspensor are closely coordinated, and imbalance causes embryonic defects or lethality (2)(3)(4). While the embryo proper gives rise to the plant, the suspensor functions during a brief period as a conduit of growth factors to the developing embryo and is subsequently eliminated by PCD (2).…”

mentioning

confidence: 99%

Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis

Bozhkov

Suárez

Filonova

et al. 2005

226

235

Programmed cell death (PCD) is indispensable for eukaryotic development. In animals, PCD is executed by the caspase family of cysteine proteases. Plants do not have close homologues of caspases but possess a phylogenetically distant family of cysteine proteases named metacaspases. The cellular function of metacaspases in PCD is unknown. Here we show that during plant embryogenesis, metacaspase mcII-Pa translocates from the cytoplasm to nuclei in terminally differentiated cells that are destined for elimination, where it colocalizes with the nuclear pore complex and chromatin, causing nuclear envelope disassembly and DNA fragmentation. The cell-death function of mcII-Pa relies on its cysteine-dependent arginine-specific proteolytic activity. Accordingly, mutation of catalytic cysteine abrogates the proteolytic activity of mcII-Pa and blocks nuclear degradation. These results establish metacaspase as an executioner of PCD during embryo patterning and provide a functional link between PCD and embryogenesis in plants. Although mcII-Pa and metazoan caspases have different substrate specificity, they serve a common function during development, demonstrating the evolutionary parallelism of PCD pathways in plants and animals.embryo suspensor ͉ metacaspase ͉ nuclear degradation P rogrammed cell death (PCD) is indispensable for normal embryo development both in animals and in plants, where temporary, surplus, or aberrantly formed tissues and organs are removed for correct pattern formation (1, 2). The key morphogenetic event in plant embryogenesis is formation of the apicalbasal pattern via establishment of the proliferating embryo proper (apical) and the terminally differentiated suspensor (basal). Developmental programs of the embryo proper and the suspensor are closely coordinated, and imbalance causes embryonic defects or lethality (2-4). While the embryo proper gives rise to the plant, the suspensor functions during a brief period as a conduit of growth factors to the developing embryo and is subsequently eliminated by PCD (2). The terminal differentiation of the embryo suspensor is the earliest manifestation of cellular suicide in plant ontogenesis. However, the molecular mechanisms that regulate PCD in plant embryos are unknown.The nucleus is the major target of cell degradation machinery during PCD. Nuclear degradation processes encompass chromatin events (i.e., chromatin condensation and DNA fragmentation) and nuclear envelope events (i.e., lobing of the nuclear surface and disassembly of nuclear pore complex) that occur simultaneously in the same cell (2, 5). The structural organization of plant and animal nuclei is conserved (6), explaining why the morphological pattern of nuclear degradation is also conserved (2). However, the molecular composition of plant and animal nuclear envelopes is not conserved (6), implying that different molecular mechanisms are responsible for nuclear envelope events during PCD in plants.In animals, nuclear degradation during PCD is executed by a caspase family of cysteine proteases...