FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot.
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ABSTRACT:
SUBMITTER: Malivert A
PROVIDER: S-EPMC8612563 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Plants absorb light energy required for photosynthesis, but excess light can damage plant cells. To protect themselves, plants have developed diverse signaling pathways which are activated under high-intensity light. Plant photoprotection mechanisms have been mainly investigated under conditions of extremely high amount of light; thus, it is largely unknown how plants manage photooxidative damage under moderate light intensities. In the present study, we found that FERONIA (FER) is a key protein that confers resistance to photooxidative stress in plants under moderate light intensity. FER-deficient mutants were highly susceptible to increasing light intensity and exhibited photobleaching even under moderately elevated light intensity (ML). Light-induced expression of stress genes was largely diminished by the fer-4 mutation. In addition, excitation pressure on Photosystem II was significantly increased in fer-4 mutants under ML. Consistently, reactive oxygen species, particularly singlet oxygen, accumulated in fer-4 mutants grown under ML. FER protein abundance was found to be elevated after exposure to ML, which is indirectly affected by the ubiquitin-proteasome pathway. Altogether, our findings showed that plants require FER-mediated photoprotection to maintain their photosystems even under moderate light intensity.
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Project description:BACKGROUND:The receptor-like kinase FEROINA (FER) plays a crucial role in controlling plant vegetative growth partially by sensing the rapid alkalinization factor (RALF) peptide. However, the role of RALF1-FER in the vegetative-reproductive growth transition remains unknown. Here, we analyze the mechanism through which FER affects the flowering time in Arabidopsis. RESULTS:We found that the FER mRNA levels exhibit an oscillating pattern with a diurnal rhythm and that the clock oscillator CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) up-regulates the expression of FER by associating with its chromatin. In addition, FER expression is regulated by clock genes, and FER also modulates the expression patterns of clock genes. Consistent with its gene expression pattern, FER positively regulates flowering by modulating the transcript accumulation and mRNA alternative splicing of certain flowering-related genes, including FLOWERING LOCUS C (FLC) and its homolog MADS AFFECTING FLOWERING (MAF). However, the RALF1 ligand negatively regulates flowering compared with FER. CONCLUSIONS:We found that FER, which is up-regulated by CCA1, controls the flowering time by regulating the transcript accumulation and mRNA alternative splicing (AS) of some important flowering genes, and these findings link FER to the floral transition.
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Project description:Exogenous mechanical perturbations on living tissues are commonly used to investigate whether cell effectors can respond to mechanical cues. However, in most of these experiments, the applied mechanical stress and/or the biological response are described only qualitatively. We developed a quantitative pipeline based on microindentation and image analysis to investigate the impact of a controlled and prolonged compression on microtubule behaviour in the Arabidopsis shoot apical meristem, using microtubule fluorescent marker lines. We found that a compressive stress, in the order of magnitude of turgor pressure, induced apparent microtubule bundling. Importantly, that response could be reversed several hours after the release of compression. Next, we tested the contribution of microtubule severing to compression-induced bundling: microtubule bundling seemed less pronounced in the katanin mutant, in which microtubule severing is dramatically reduced. Conversely, some microtubule bundles could still be observed 16 h after the release of compression in the spiral2 mutant, in which severing rate is instead increased. To quantify the impact of mechanical stress on anisotropy and orientation of microtubule arrays, we used the nematic tensor based FibrilTool ImageJ/Fiji plugin. To assess the degree of apparent bundling of the network, we developed several methods, some of which were borrowed from geostatistics. The final microtubule bundling response could notably be related to tissue growth velocity that was recorded by the indenter during compression. Because both input and output are quantified, this pipeline is an initial step towards correlating more precisely the cytoskeleton response to mechanical stress in living tissues.
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Project description:Plant cell expansion is driven by turgor pressure and regulated by hormones. How plant cells avoid cell wall rupture during hormone-induced cell expansion remains a mystery. Here we show that brassinosteroid (BR), while stimulating cell elongation, promotes the plasma membrane (PM) accumulation of the receptor kinase FERONIA (FER), which monitors cell wall damage and in turn attenuates BR-induced cell elongation to prevent cell rupture. The GSK3-like kinase BIN2 phosphorylates FER, resulting in reduced FER accumulation and translocation from endoplasmic reticulum to PM. By inactivating BIN2, BR signaling promotes dephosphorylation and increases PM accumulation of FER, thereby enhancing the surveillance of cell wall integrity. Our study reveals a vital signaling circuit that coordinates hormone signaling with mechanical sensing to prevent cell bursting during hormone-induced cell expansion.
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Project description:The role of mechanical signals in cell identity determination remains poorly explored in tissues. Furthermore, because mechanical stress is widespread, mechanical signals are difficult to uncouple from biochemical-based transduction pathways. Here we focus on the homeobox gene SHOOT MERISTEMLESS (STM), a master regulator and marker of meristematic identity in Arabidopsis. We found that STM expression is quantitatively correlated to curvature in the saddle-shaped boundary domain of the shoot apical meristem. As tissue folding reflects the presence of mechanical stress, we test and demonstrate that STM expression is induced after micromechanical perturbations. We also show that STM expression in the boundary domain is required for organ separation. While STM expression correlates with auxin depletion in this domain, auxin distribution and STM expression can also be uncoupled. STM expression and boundary identity are thus strengthened through a synergy between auxin depletion and an auxin-independent mechanotransduction pathway at the shoot apical meristem.
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Project description:The control of cell position and division act in concert to dictate multicellular organization in tissues and organs. How these processes shape global order and molecular movement across organs is an outstanding problem in biology. Using live 3D imaging and computational analyses, we extracted networks capturing cellular connectivity dynamics across the Arabidopsis shoot apical meristem (SAM) and topologically analyzed the local and global properties of cellular architecture. Locally generated cell division rules lead to the emergence of global tissue-scale organization of the SAM, facilitating robust global communication. Cells that lie upon more shorter paths have an increased propensity to divide, with division plane placement acting to limit the number of shortest paths their daughter cells lie upon. Cell shape heterogeneity and global cellular organization requires KATANIN, providing a multiscale link between cell geometry, mechanical cell-cell interactions, and global tissue order.
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Project description:Cells maintain integrity despite changes in their mechanical properties elicited during growth and environmental stress. How cells sense their physical state and compensate for cell-wall damage is poorly understood, particularly in plants. Here we report that FERONIA (FER), a plasma-membrane-localized receptor kinase from Arabidopsis, is necessary for the recovery of root growth after exposure to high salinity, a widespread soil stress. The extracellular domain of FER displays tandem regions of homology with malectin, an animal protein known to bind di-glucose in vitro and important for protein quality control in the endoplasmic reticulum. The presence of malectin-like domains in FER and related receptor kinases has led to widespread speculation that they interact with cell-wall polysaccharides and can potentially serve a wall-sensing function. Results reported here show that salinity causes softening of the cell wall and that FER is necessary to sense these defects. When this function is disrupted in the fer mutant, root cells explode dramatically during growth recovery. Similar defects are observed in the mur1 mutant, which disrupts pectin cross-linking. Furthermore, fer cell-wall integrity defects can be rescued by treatment with calcium and borate, which also facilitate pectin cross-linking. Sensing of these salinity-induced wall defects might therefore be a direct consequence of physical interaction between the extracellular domain of FER and pectin. FER-dependent signaling elicits cell-specific calcium transients that maintain cell-wall integrity during salt stress. These results reveal a novel extracellular toxicity of salinity, and identify FER as a sensor of damage to the pectin-associated wall.
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Project description:Accumulating evidence indicates that early and essential events for receptor-like kinase (RLK) function involve both autophosphorylation and substrate phosphorylation. However, the structural and biochemical basis for these events is largely unclear. Here, we used RLK FERONIA (FER) as a model and crystallized its core kinase domain (FER-KD) and two FER-KD mutants (K565R, S525A) in complexes with ATP/ADP and Mg2+ in the unphosphorylated state. Unphosphorylated FER-KD was found to adopt an unexpected active conformation in its crystal structure. Moreover, unphosphorylated FER-KD mutants with reduced (S525A) or no catalytic activity (K565R) also adopt similar active conformations. Biochemical studies revealed that FER-KD is a dual-specificity kinase, and its autophosphorylation is accomplished via an intermolecular mechanism. Further investigations confirmed that initiating substrate phosphorylation requires autophosphorylation of the activation segment on T696, S701, and Y704. This study reveals the structural and biochemical basis for the activation and regulatory mechanism of FER, providing a paradigm for the early steps in RLK signaling initiation.
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Project description:Acetylation of ?-tubulin at lysine 40 (K40) is a well-conserved posttranslational modification that marks long-lived microtubules but has poorly understood functional significance. Recently, ?TAT1, a member of the Gcn5-related N-acetyltransferase superfamily, has been identified as an ?-tubulin acetyltransferase in ciliated organisms. Here, we explored the function of ?TAT1 with the aim of understanding the consequences of ?TAT1-mediated microtubule acetylation. We demonstrate that ?-tubulin is the major target of ?TAT1 but that ?TAT1 also acetylates itself in a regulatory mechanism that is required for effective modification of tubulin. We further show that in mammalian cells, ?TAT1 promotes microtubule destabilization and accelerates microtubule dynamics. Intriguingly, this effect persists in an ?TAT1 mutant with no acetyltransferase activity, suggesting that interaction of ?TAT1 with microtubules, rather than acetylation per se, is the critical factor regulating microtubule stability. Our data demonstrate that ?TAT1 has cellular functions that extend beyond its classical enzymatic activity as an ?-tubulin acetyltransferase.
| S-EPMC3592022 | biostudies-literature
Project description:BackgroundThe best-studied arrangement of microtubules is that organized by the centrosome, a cloud of microtubule nucleating and anchoring proteins is clustered around centrioles. However, noncentrosomal microtubule arrays are common in many differentiated cells, including neurons. Although microtubules are not anchored at neuronal centrosomes, it remains unclear whether the centrosome plays a role in organizing neuronal microtubules. We use Drosophila as a model system to determine whether centrosomal microtubule nucleation is important in mature neurons.ResultsIn developing and mature neurons, centrioles were not surrounded by the core nucleation protein γ-tubulin. This suggests that the centrioles do not organize functional centrosomes in Drosophila neurons in vivo. Consistent with this idea, centriole position was not correlated with a specific region of the cell body in neurons, and growing microtubules did not cluster around the centriole, even after axon severing when the number of growing plus ends is dramatically increased. To determine whether the centrosome was required for microtubule organization in mature neurons, we used two approaches. First, we used DSas-4 centriole duplication mutants. In these mutants, centrioles were present in many larval sensory neurons, but they were not fully functional. Despite reduced centriole function, microtubule orientation was normal in axons and dendrites. Second, we used laser ablation to eliminate the centriole, and again found that microtubule polarity in axons and dendrites was normal, even 3 days after treatment.ConclusionWe conclude that the centrosome is not a major site of microtubule nucleation in Drosophila neurons, and is not required for maintenance of neuronal microtubule organization in these cells.
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