A Role for Auxin in Ethylene-Dependent Inducible Aerenchyma Formation in Rice Roots.
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ABSTRACT:
SUBMITTER: Yamauchi T
PROVIDER: S-EPMC7284992 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Although the cross-talk between auxin and ethylene has been described during plant development, the role played by auxin upon gene expression during aerenchyma formation is poorly understood. Root aerenchyma formation results from the opening of gas spaces in the cortex. It is part of a developmental program (constitutive) or due to ethylene treatment or abiotic stress (induced) such as flooding and nutrient starvation. This process relies on programmed cell death and cell wall modifications. Here we followed development of aerenchyma formation in sugarcane along 5 cm from the root apex. As a constitutive process, the aerenchyma formation was observed in the cortex from the 3rd cm onwards. This occurred despite 1-methylcyclepropene (1-MCP) treatment, an inhibitor of ethylene perception. However, this process occurred while ethylene (and auxin) levels decreased. Within the aerenchyma formation zone, the concentration of ethylene is lower in comparison to the concentration in maize. Besides, the ratio between both hormones (ethylene and auxin) was around 1:1. These pieces of evidence suggest that ethylene sensitivity and ethylene-auxin balance may play a role in the formation of aerenchyma. Furthermore, the transcriptional analysis showed that genes related to cell expansion are up-regulated due to 1-MCP treatment. Our results help explaining the regulation of the formation constitutive aerenchyma in sugarcane.
| S-EPMC5927678 | biostudies-literature
Project description:The longitudinal pattern of root aerenchyma formation of its relationship with the function of adventitious roots in rice remains unclear. In this study, the percentage of the aerenchyma area to the cross-sectional area (i.e., aerenchyma percentage) was fit with four non-linear models, namely, W0-Gompertz, Ti-Gompertz, logistic, and von Bertalanffy. Goodness-of-fit criteria such as the R 2, the Akaike information criterion (AIC), and the Bayesian information criterion (BIC) were used to select the model. The bias of the parameters was evaluated using the difference between the ordinary least squares-based parameter estimates and the mean of 1,000 bootstrap-based parameter estimates and the symmetry of the distributions of these parameters. The results showed that the Ti-Gompertz model, which had a high goodness-of-fit with an R 2 close to 1, lower AIC and BIC values, parameter estimates close to being unbiased, and good linear approximation, provided the best fit for the longitude pattern of rice aerenchyma formation with different root lengths among the competing models. Using the second- and third-order derivatives according to the distance from the root apex, the critical points of Ti-Gompertz were calculated. The rapid stage for aerenchyma formation was from the maximum acceleration point (1.38-1.76 cm from the root apex) to the maximum deceleration point (3.13-4.19 cm from the root apex). In this stage, the aerenchyma percentage increased by 5.3-15.7% per cm, suggesting that the cortical cells tended to die rapidly for the aerenchyma formation rather than for the respiration cost during this stage. Meanwhile, the volume of the aerenchyma of the entire roots could be computed using the integral function of the Ti-Gompertz model. We proposed that the longitudinal pattern of root aerenchyma formation modeled by the Ti-Gompertz model helped to deeply understand the relationship between the anatomical traits and physiological function in rice adventitious roots.
| S-EPMC8669396 | biostudies-literature
Project description:Background and aimsMany wetland species form aerenchyma and a barrier to radial O(2) loss (ROL) in roots. These features enhance internal O(2) diffusion to the root apex. Barrier formation in rice is induced by growth in stagnant solution, but knowledge of the dynamics of barrier induction and early anatomical changes was lacking.MethodsROL barrier induction in short and long roots of rice (Oryza sativa L. 'Nipponbare') was assessed using cylindrical root-sleeving O(2) electrodes and methylene blue indicator dye for O(2) leakage. Aerenchyma formation was also monitored in root cross-sections. Microstructure of hypodermal/exodermal layers was observed by transmission electron microscopy (TEM).Key resultsIn stagnant medium, barrier to ROL formation commenced in long adventitious roots within a few hours and the barrier was well formed within 24 h. By contrast, barrier formation took longer than 48 h in short roots. The timing of enhancement of aerenchyma formation was the same in short and long roots. Comparison of ROL data and subsequent methylene blue staining determined the apparent ROL threshold for the dye method, and the dye method confirmed that barrier induction was faster for long roots than for short roots. Barrier formation might be related to deposition of new electron-dense materials in the cell walls at the peripheral side of the exodermis. Histochemical staining indicated suberin depositions were enhanced prior to increases in lignin.ConclusionsAs root length affected formation of the barrier to ROL, but not aerenchyma, these two acclimations are differentially regulated in roots of rice. Moreover, ROL barrier induction occurred before histochemically detectable changes in putative suberin and lignin deposits could be seen, whereas TEM showed deposition of new electron-dense materials in exodermal cell walls, so structural changes required for barrier functioning appear to be more subtle than previously described.
| S-EPMC3002478 | biostudies-literature
Project description:γ-Aminobutyric acid (GABA) is a widely distributed non-protein amino acid mediated the regulation of nitrate uptake and Al3+ tolerance in plants. However, there are few reports about the involvement of GABA in the regulation of iron (Fe) acquisition and translocation. Here, we show that GABA regulates Fe homeostasis in rice seedlings. Exogenous GABA decreased the chlorophyll concentration in leaves, with or without Fe supply. Over-expression of glutamate decarboxylase (GAD) gene, coding a crucial enzyme of GABA production, elevated endogenous GABA content and caused more leaf chlorosis than wild type (Nipponbare). GABA inhibited Fe transportation from roots to shoots and GABA application elevated the expression levels of Fe deficiency (FD)-related genes under conditions of Fe-sufficiency (FS), suggesting that GABA is a regulator of Fe translocation. Using Perls' blue staining, we found that more ferric iron (Fe3+) was deposited in the epidermal cells of roots treated with GABA compared with control roots. Anatomic section analysis showed that GABA treatment induced more aerenchyma formation compared with the control. Aerenchyma facilitated the oxidization of soluble ferrous iron (Fe2+) into insoluble Fe3+, resulted in Fe precipitation in the epidermis, and inhibited the transportation of Fe from roots to shoots.
| S-EPMC7795648 | biostudies-literature
Project description:Auxin distribution is essential for determining root developmental patterns. The formation of lateral roots and constitutive aerenchyma, which is a gas space developed through cell death, is regulated by auxin in rice (Oryza sativa). However, it is unclear whether the involvement of auxin in constitutive aerenchyma formation is conserved in other species. In this study, we found that constitutive aerenchyma formation was regulated by auxin in the nodal roots of Zea nicaraguensis, a wild relative of maize (Zea mays ssp. mays) grown naturally on frequently flooded coastal plains. Subsequent gravistimulation (root rotation) experiments showed opposite patterns of aerenchyma and lateral root formation. Lateral root formation on the convex side of rotated roots is known to be stimulated by a transient increase in auxin level in the pericycle. We found that aerenchyma formation was accelerated in the cortex on the concave side of the rotated nodal roots of Z. nicaraguensis. A cortex-specific expression analysis of auxin-responsive genes suggested that the auxin level was higher on the concave side than on the convex side. These results suggest that asymmetric auxin distribution underlies the regulation of aerenchyma and lateral root formation in the nodal roots of Z. nicaraguensis. As aerenchyma reduces the respiratory cost of the roots, constitutive aerenchyma on the concave side of the nodal root may balance resource allocation, thereby contributing to the uptake of water and nutrients by newly formed lateral roots. Our study provides insights into auxin-dependent asymmetric root patterning such as that of gravistimulation and hydropatterning response.
| S-EPMC10154625 | biostudies-literature
Project description:Background and aimsAerenchyma develops in different plant organs and leads to the formation of intercellular spaces that can be used by the plant to transport volatile substances. Little is known about the role of cell walls in this process, although the mechanism of aerenchyma formation is known to involve programmed cell death and some cell wall modifications. We assessed the role that cell wall-related mechanisms might play in the formation of aerenchyma in sugarcane roots.MethodsSections of roots (5?cm) were subjected to microtomography analysis. These roots were divided into 1-cm segments and subjected to cell wall fractionation. We performed analyses of monosaccharides, oligosaccharides and lignin and glycome profiling. Sections were visualized by immunofluorescence and immunogold labelling using selected monoclonal antibodies against polysaccharide epitopes according to the glycome profiles.Key resultsDuring aerenchyma formation, gas spaces occupied up to 40 % of the cortex cross-section within the first 5?cm of the root. As some of the cortex cells underwent dissolution of the middle lamellae, leading to cell separation, cell expansion took place along with cell death. Mixed-linkage ?-glucan was degraded along with some homogalacturonan and galactan, culminating in the formation of cell wall composites made of xyloglucan, arabinoxylans, cellulose and possibly lignin.ConclusionThe composites formed seem to play a role in the physical-chemical properties of the gas chambers, providing mechanical resistance to forces acting upon the root and at the same time decreasing permeability to gases.
| S-EPMC5714247 | biostudies-literature
Project description:Small RNAs comprise three families of noncoding regulatory RNAs that control gene expression by blocking mRNA translation or leading to mRNA cleavage. Such post-transcriptional negative regulation is relevant for both plant development and environmental adaptations. An important biotechnological application of miRNA identification is the discovery of regulators and effectors of cell wall degradation, which can improve/facilitate hydrolysis of cell wall polymers for second-generation bioethanol production. The recent characterization of plant innate cell wall modifications occurring during root aerenchyma development triggered by ethylene led to the possibility of prospection for mechanisms of cell wall disassembly in sugarcane. By using next-generation sequencing, 39 miRNAs were identified in root segments along the process of aerenchyma development. Among them, 31 miRNAs were unknown to the sugarcane miRBase repository but previously identified as produced by its relative Sorghum bicolor. Key putative targets related to signal transduction, carbohydrate metabolic process, and cell wall organization or biogenesis were among the most representative gene categories targeted by miRNA. They belong to the subclasses of genes associated with the four modules of cell wall modification in sugarcane roots: cell expansion, cell separation, hemicellulose, and cellulose hydrolysis. Thirteen miRNAs possibly related to ethylene perception and signaling were also identified. Our findings suggest that miRNAs may be involved in the regulation of cell wall degradation during aerenchyma formation. This work also points out to potential molecular tools for sugarcane improvement in the context of second-generation biofuels.
| S-EPMC7098396 | biostudies-literature
Project description:Under waterlogged conditions, roots of gramineous plants form lysigenous aerenchyma (internal gas spaces) by inducing the death of cortical cells. Rice (Oryza sativa) roots induce aerenchyma formation through ethylene- and reactive oxygen species (ROS)-mediated signaling. Metallothionein (MT) is a small, cysteine-rich protein that acts as a ROS scavenger. In rice roots, the expression of MT1a, MT1b, MT1c and MT1Ld were higher than those of the other MT genes. In the root cortex, where aerenchyma forms exclusively, the expression of MT1a, MT1b and MT1Ld was reduced prior to aerenchyma formation. These findings suggest that ROS accumulation in the cortex, which is aided by downregulation of MT1 genes, is needed for aerenchyma formation in rice roots.
| S-EPMC5703249 | biostudies-literature
Project description:Understanding plant adaptation mechanisms to prolonged water immersion provides options for genetic modification of existing crops to create cultivars more tolerant of periodic flooding. An important advancement in understanding flooding adaptation would be to elucidate mechanisms, such as aerenchyma air-space formation induced by hypoxic conditions, consistent with prolonged immersion. Lysigenous aerenchyma formation occurs through programmed cell death (PCD), which may entail the chemical modification of polysaccharides in root tissue cell walls. We investigated if a relationship exists between modification of pectic polysaccharides through de-methyl esterification (DME) and the formation of root aerenchyma in select Fabaceae species. To test this hypothesis, we first characterized the progression of aerenchyma formation within the vascular stele of three different legumes-Pisum sativum, Cicer arietinum, and Phaseolus coccineus-through traditional light microscopy histological staining and scanning electron microscopy. We assessed alterations in stele morphology, cavity dimensions, and cell wall chemistry. Then we conducted an immunolabeling protocol to detect specific degrees of DME among species during a 48-hour flooding time series. Additionally, we performed an enzymatic pretreatment to remove select cell wall polymers prior to immunolabeling for DME pectins. We were able to determine that all species possessed similar aerenchyma formation mechanisms that begin with degradation of root vascular stele metaxylem cells. Immunolabeling results demonstrated DME occurs prior to aerenchyma formation and prepares vascular tissues for the beginning of cavity formation in flooded roots. Furthermore, enzymatic pretreatment demonstrated that removal of cellulose and select hemicellulosic carbohydrates unmasks additional antigen binding sites for DME pectin antibodies. These results suggest that additional carbohydrate modification may be required to permit DME and subsequent enzyme activity to form aerenchyma. By providing a greater understanding of cell wall pectin remodeling among legume species, we encourage further investigation into the mechanism of carbohydrate modifications during aerenchyma formation and possible avenues for flood-tolerance improvement of legume crops.
| S-EPMC7008352 | biostudies-literature
Project description:Understanding how developmental and environmental signals are integrated to produce specific responses is one of the main challenges of modern biology. Hormones and, most importantly, interactions between different hormones serve as crucial regulators of plant growth and development, playing central roles in the coordination of internal developmental processes with the environment. Herein, a combination of physiological, genetic, cellular, and whole-genome expression profiling approaches has been employed to investigate the mechanisms of interaction between two key plant hormones, ethylene and auxin. Quantification of the morphological effects of ethylene and auxin in a variety of mutant backgrounds indicates that auxin biosynthesis, transport, signaling and response are required for the ethylene-induced growth inhibition in roots but not in hypocotyls. Analysis of the activation of early auxin and ethylene responses at cellular level, as well as of global changes in gene expression in the wild type versus auxin and ethylene mutants, suggests a simple mechanistic model for the interaction between these two hormones in roots. This model not only implies existence of several levels of interaction but also provides a likely explanation for the strong ethylene response defects observed in auxin mutants. Keywords: Genetic modification. Plant hormone response
2007-07-13 | GSE7432 | GEO