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Aerenchyma Formation in Plants
Abstract and Figures
Aerenchyma enhances internal aeration between, and within, shoots and roots. Aerenchyma formation is therefore important for the adaptation of plants in environments with excess water, such as plants with roots in waterlogged soils or submerged shoots. Aerenchyma can form in primary tissues (primary aerenchyma) and in secondary tissues (secondary aerenchyma). Primary tissues have two main types of aerenchyma: schizogenous aerenchyma and lysigenous aerenchyma. Both types provide enlarged spaces for gas-phase diffusion. Schizogenous aerenchyma is formed by the separation of adjacent files (radial rows) of cortical cells and by enlargement of existing intercellular spaces through cell division and differential cell enlargement. By contrast, lysigenous aerenchyma results from the collapse and lysis of files of cortical cells via programmed cell death. Secondary aerenchyma differentiates from phellogen, cambium, and pericycle in stems, hypocotyls, or roots of some dicots to form a gas-filled and low-resistance pathway for gas movement. Presently, the mechanisms of schizogenous and secondary aerenchyma formation are less well understood than the mechanisms of lysigenous aerenchyma formation. Here, we summarize the characteristics of primary aerenchyma (schizogenous and lysigenous aerenchymas) and secondary aerenchyma types, and present recent advances in understanding the mechanisms of lysigenous aerenchyma formation.
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... Abnormalities in somatic embryos of T. cacao are frequently found in other works, where the researchers identified somatic embryos with more than two cotyledons, fasciation and fusion of more than two cotyledons, but the behavior of these abnormal SE in germination is not known 26 . The histological and scanning electron microscopy analysis of abnormal SE revealed abnormal cell division in the provascular tissue originating from the provascular initial cells 27 and some intercellular cavity formation in the embryo body similar to cavity formation through both schizogenous or lysigenous aerenchyma formation in plants when they are exposed to flooding conditions 28 . Schizogenous aerenchyma is formed by cell division and enlargement of intercellular spaces of cortical cells where there is a separation between the adjacent cell files, whereas lysigenous aerenchyma is formed by the collapse or lysis of the cortical cell files via programmed cell death (PCD) 28 . ...
... The histological and scanning electron microscopy analysis of abnormal SE revealed abnormal cell division in the provascular tissue originating from the provascular initial cells 27 and some intercellular cavity formation in the embryo body similar to cavity formation through both schizogenous or lysigenous aerenchyma formation in plants when they are exposed to flooding conditions 28 . Schizogenous aerenchyma is formed by cell division and enlargement of intercellular spaces of cortical cells where there is a separation between the adjacent cell files, whereas lysigenous aerenchyma is formed by the collapse or lysis of the cortical cell files via programmed cell death (PCD) 28 . ...
... In this study we identified genes differentially methylated in ZE, normal and abnormal SE with important functions in PCD, specifically in cell response to hypoxia, calcium signaling and production of peroxidases which is one of the important reactive oxygen species (ROS) key modulator of plant growth and development, and stress adaptation. Those findings can explain the presence of cavities in the embryo body of abnormal SE, a probably product of lysigeny via PCD for lack of oxygen in the in vitro culture environment, inducing the death of the tissue mediated by ROS 28 . ...
Propagation by somatic embryogenesis in Theobroma cacao has some issues to be solved, as many morphologically abnormal somatic embryos that do not germinate into plants are frequently observed, thus hampering plant production on a commercial scale. For the first time the methylome landscape of T. cacao somatic embryogenesis was examined, using whole-genome bisulfite sequencing technique, with the aim to understand the epigenetic basis of somatic embryo abnormalities . We identified 873 differentially methylated genes (DMGs) in the CpG context between zygotic embryos, normal and abnormal somatic embryos, with important roles in development, programmed cell death, oxidative stress, and hypoxia induction, which can help to explain the morphological abnormalities of somatic embryos. We also identified the role of ethylene and its precursor 1-aminocyclopropane-1-carboxylate in several biological processes, such as hypoxia induction, cell differentiation and cell polarity, that could be associated to the development of abnormal somatic embryos. The biological processes and the hypothesis of ethylene and its precursor involvement in the somatic embryo abnormalities in cacao are discussed.
... However, secondary aerenchyma is newly differentiated from secondary meristem (i.e., phellogen or cork cambium) 7 . Secondary aerenchyma is classi ed into the aerenchymatous phellem (AP), differentiated inward from phellogen, and the porous secondary cortex, differentiated outward from phellogen 7 . ...
... However, secondary aerenchyma is newly differentiated from secondary meristem (i.e., phellogen or cork cambium) 7 . Secondary aerenchyma is classi ed into the aerenchymatous phellem (AP), differentiated inward from phellogen, and the porous secondary cortex, differentiated outward from phellogen 7 . AP is a white, spongy, and highly porous tissue, and transports oxygen to roots under waterlogged conditions 8, 9 . ...
Aerenchymatous phellem (AP) is important for internal aeration and adaptation to waterlogging in plants. Herein, the extensive accumulation of triterpenoids such as lupeol and betulinic acid was identified in AP. However, the biological and physiological roles of these triterpenoids in plants are largely unknown. Lupeol is converted from 2,3-oxidosqualene by lupeol synthase (LUS) and oxidized to betulinic acid. Functional analysis of LUS genes in soybean revealed that GmLUS1 is crucial for triterpenoid biosynthesis in AP. Lupeol and betulinic acid were found to be the major components of epicuticular wax on the surface of AP cells, and they contributed to tissue hydrophobicity and oxygen transport to roots. Additionally, the lus1 mutant produced a shallow root system due to less oxygen transport via AP under waterlogged conditions. In conclusion, triterpenoid accumulation in AP aids internal aeration and root development for adaptation to waterlogging.
... Aerenchyma can develop constitutively (even in drained soil) and/or can be induced by soil waterlogging (Yamauchi et al., 2013;Takahashi et al., 2014;Gong et al., 2019;Pedersen et al., 2021). For the constitutive aerenchyma formation, it was only reported in rice that constitutive aerenchyma formation was partially suppressed by the 1-methylcyclopropene (1-MCP, an ethylene perception inhibitor). ...
As global warming and climate change is occurring all over the world, waterlogging/flooding has become a serious stress for plant growth. The metabolic changes and morphological changes such as aerenchyma formation, adventitious root formation and shoot/internodes elongation are involved in plants to survive under flooded condition. Ethylene is the first signal to initiate these metabolic and morphological changes. Auxin mainly regulates adventitious root formation and aerenchyma formation through its transport and signal transduction. Gibberellin has been reported to have a major role in controlling shoot elongation and adventitious root formation, while abscisic acid is considered as a negative regulator of the morphological development upon flooding, such as shoot/internode elongation and adventitious root emergence. The interaction between ethylene and other hormones is also important in flooding responses. Ethylene regulates aerenchyma formation through reactive oxygen species-induced programmed cell death, and it acts synergistically with auxin to control adventitious root formation. It also acts synergistically with gibberellin and antagonistically with abscisic acid in regulating adventitious root formation and shoot/internode elongation. In this review, we summarize recent progress in hormonal regulation of flooding responses in plants.
Our book consists of a collection of 22 chapters with studies developed in one of the most important basins of the state of Rio Grande do Norte, the Basin Apodi-Mossoró River Hydrographic Station (BHAM). the chapters of the book address: (i) the main environmental aspects, economic and social aspects of the basin; (ii) morphometric analysis elaborated by digital elevation models and geographic information systems; (iii) the characterization limnology of aquatic ecosystems at BHAM before and after the period of prolonged drought, which affected large part of the northeastern semi-arid region between the years from 2012 and 2017; (iv) the degree of metal contamination weights of the BHAM aquatic environments and the relation their concentrations with the use and occupation of the basin; (v) aquatic communities (bacterioplankton, phytoplankton, aquatic macrophytes, zooplankton, molluscs and fish) and (vi) the main aspects related the production of salt and shrimp in the estuary of the river Apodi-Mossoró. In the last chapter of the book, the
two ecosystem models with potential application in the Brazilian semi-arid region, in order to carry out simulations and predictions that can help in decisions management and sustainable use of water resources.
Distributed in different elevations of the intertidal zone, mangrove plants suffer different periods of flooding, and with varied adaptability to waterlogging from the physiological structure to the metabolic mechanism. Associated with species distribution, transcriptome sequencing was performed to explore the interspecific differences of molecular response mechanisms among Avicennia marina , Aegiceras corniculatum , and Bruguiera gymnorrhiza under waterlogging stress. Results showed that the counts of differentially expressed genes (DEGs) in A. Marina were the highest after stress, followed by Ae. corniculatum and B. gymnorrhiza . It was found that the functions of genes with high differential expression folds (more than eight folds) in the three plants could be classified into four categories: structural regulation, transport, biosynthesis, and protection. It was also found that A. Marina has strong regulation ability in the metabolic process, which can guarantee energy supply and maintain active biosynthesis under waterlogging conditions. In addition, A. Marina was activated in the ethylene synthesis pathway to promote aerenchyma formation and to avoid root tissue hypoxia. Being different from A. Marina and B. gymnorrhiza , Ae. corniculatum down-regulated the XET , SAMS , and ACCO genes, which were involved in the cell wall regulation or ethylene formation that might indicate a different adaptive mechanism. Alcohol dehydrogenase ( ADH ) and lactate dehydrogenase ( LDH ) were cloned from A. Marina , Ae. corniculatum , and B. gymnorrhiza . The cloned genes were named as AmADH , AmLDH , AcADH , AcLDH , BgADH , and BgLDH , respectively. qRT-PCR detection verified that LDH s and ADH s were involved in the response of mangrove plants to waterlogging stress, and interspecific difference was observed. The expressions of AcADH and AcLDH were the most prominent. Combined with transcriptome, it was considered that Ae. corniculatum was more dependent on the expression of AcADH and AcLDH that might compensate the weakness of cell wall regulation, whereas A. Marina was more dependent on the regulation of cell structure reversely.
The perennial Cyperus rotundus (Cyperaceae) is a noxious weed worldwide that tolerates the extreme environments of the Three Gorges Reservoir, China. Using brightfield and epifluorescence microscopy, we investigated the anatomical and histochemical features that allow this species to thrive in amphibious environments. The apoplastic barriers of C. rotundus consisted of an endodermis, a uniseriate exodermis, and a cuticle in the roots, rhizomes, and culms, respectively, as well as suberized stele and primary xylem poles. These barriers may help C. rotundus to retain oxygen and control water-solute exchanges under anoxic conditions. The mechanical tissues of C. rotundus included lignified sclerenchyma rings and sclerenchyma fibers in the roots, shoots, rhizomes, and tubers. The air spaces had lysed aerenchyma in the roots, leaves, and rhizomes, while schizogenous aerenchyma was observed in the culms. Neither lysed nor schizogenous aerenchyma was found in the tubers. C. rotundus is a typical C4 species with Kranz anatomy; chloroplasts were present in the inner sheaths and parenchymatous sheaths. Thus, our analyses identified several anatomical and histochemical features that may facilitate the adaptive success of C. rotundus in amphibious environments.
The aquatic legume Neptunia plena (L.) Benth. was grown in non-aerated water culture or vermiculite. Growth,
nodulation, nitrogen fixation and nodule physiology were investigated. Over an 80-d period, plants grew and fixed nitrogen and carbon equally well in both rooting media, although distribution of growth between plant parts varied. Total nodule dry weights and volumes were similar but vermiculite-grown plants had three times as many (smaller) nodules than those grown in water. Oxygen diffusion resistance of nodules exposed to 21% oxygen and 10% acetylene did not differ significantly. Both treatments showed similar declines in root respiration and acetylene reduction activity (approx. 10%) when root systems were exposed to stepped decreases and increases in rhizosphere oxygen concentration. However, nitrogenase activity of aquatically grown plants was irreversibly inhibited by rapid exposure of nodules to ambient air, whereas vermiculite-grown plants were unaffected. Aeration of water-cultured N. plena reduced stem length (but not mass) and number of nodules per plant. The concentration of nitrogen in leaves was also greatly reduced. Gentle agitation of the water culture doubled plant growth and increased nitrogen fixation by 163%. Possible O2 transport pathways from the shoot atmosphere to roots and nodules are discussed.
The aquatic legume Neptunia plena (L.) Benth. was grown in non-aerated water culture or vermiculite. Growth, nodulation, nitrogen fixation and nodule physiology were investigated. Over an 80-d period, plants grew and fixed nitrogen and carbon equally well in both rooting media, although distribution of growth between plant parts varied. Total nodule dry weights and volumes were similar but vermiculite-grown plants had three times as many (smaller) nodules than those grown in water. Oxygen diffusion resistance of nodules exposed to 21% oxygen and 10% acetylene did not differ significantly. Both treatments showed similar declines in root respiration and acetylene reduction activity (approx. 10%) when root systems were exposed to stepped decreases and increases in rhizosphere oxygen concentration. However, nitrogenase activity of aquatically grown plants was irreversibly inhibited by rapid exposure of nodules to ambient air, whereas vermiculite-grown plants were unaffected. Aeration of water-cultured N. plena reduced stem length (but not mass) and number of nodules per plant. The concentration of nitrogen in leaves was also greatly reduced. Gentle agitation of the water culture doubled plant growth and increased nitrogen fixation by 163%. Possible O 2 transport pathways from the shoot atmosphere to roots and nodules are discussed.
Flooding results in major changes in the soil environment. The slow diffusion rate of gases in water limits the oxygen supply, which affects aerobic root respiration as well as many (bio)geochemical processes in the soil. Plants from habitats subject to flooding have developed several ways to acclimate to these growth-inhibiting conditions, ranging from pathways that enable anaerobic metabolism to specific morphological and anatomical structures that prevent oxygen shortage. In order to acclimate in a timely manner, it is crucial that a flooding event is accurately sensed by the plant. Sensing may largely occur in two ways: by the decrease of oxygen concentration, and by an increase in ethylene. Although ethylene sensing is now well understood, progress in unraveling the sensing of oxygen has been made only recently. With respect to the signal-transduction pathways, two types of acclimation have received most attention. Aerenchyma formation, to promote gas diffusion through the roots, seems largely under control of ethylene, whereas adventitious root development appears to be induced by an interaction between ethylene and auxin. Parts of these pathways have been described for a range of species, but a complete overview is not yet available. The use of molecular-genetic approaches may fill the gaps in our knowledge, but a lack of suitable model species may hamper further progress.
Nodulated seedlings of Viminaria juncea were raised in free-draining or flooded sand culture. Unflooded seedlings developed limited amounts of aerenchyma in lower stem, root and nodules, and responded to flooding by accelerated aerenchyma production and, after 10 days, by formation of pneumatophores from their near-surface lateral roots. Continuously flooded seedlings showed earlier and greater development of aerenchyma and pneumatophores, and had their nodules and roots restricted to the upper 10 cm of the rooting medium. Aerenchyma was developed from an inner cambium, distinct from the outer phellogen which subsequently developed on older parts of stem, root and nodules. Gas contents of plant parts varied from 4-8% for organs with little aerenchyma to over 30% for the aerenchyma-invested basal stem and root of continuously flooded seedlings. A role of the sheaths of aerenchyma in gaseous exchange between aerial environment and nodulated root was demonstrated by gas injection experiments, in situ C2H2 reduction assays and 15N2 feeding experiments on intact plants with flooded roots. Samples of gas removed from the aerenchyma of plants exposed to C2H2 contained up to 14 times the amount of C2H2 and 4 times the amount of CO2 than in the atmosphere of the assay chamber, indicating that gas exchange for both N2 fixation and respiration occurred via the aerenchyma. Previously unflooded, 12-week seedlings exposed to 14 days flooding gained as much dry matter and total N in the 2-week treatment as did control unflooded plants, but 21-week continuously flooded seedlings showed only half the dry matter and nitrogen gains of similarly aged unflooded seedlings. Observations on the seasonal growth, nodulation and pneumatophore development of natural populations of the species were discussed in relation to the above findings.
This chapter illustrates the developments in the field of aeration since 1960, which have culminated in the modeling of the oxygen movements within the plant. The chapter collates the mathematical approaches to the aeration process and explains the concepts of modeling in a simplified manner. It is noted that the environment exerts a considerable influence on the directional flow of the respiratory gases within the plant and the directional exchange with the atmosphere. Oxygen can enter the plant body in a variety of ways. In non-aquatic species, the stomata and lenticels provide paths of low resistance for the entry and exit of both oxygen and carbon dioxide. In submerged astomatal aquatics, surface permeabilities are sufficiently high to allow the necessary gas transference. Plants rooted in unsaturated soils are exposed to an oxygen-rich environment over the greater part of their shoot and root surfaces. Oxygen enters the plant in the combined state as water. As water, it is transported from root to shoot in the xylem where a proportion is finally released into the liquid phase within the chloroplasts during the photolysis stage of photosynthesis.
The periderm of Ludwigia octovalvis swells readilly when immersed in water. In non-flooded individuals the periderm is very compact, composed of typical brick-shaped, thick-walled phellem cells, without intercellular spaces, and a maximal radial length of 40 µm. The periderm of flooded individuals is very loose, with sausage-shaped, thin-walled phellem cells .reaching a maximum length of 280 µm and with long intercellular spaces between them. Phellem cells of flooded plants showed elongation very early in their differentiation from phellogen cells, forming slight protuberances which increased in size with increasing distance from the phellogen. The protuberances grew predominantly in the radial direction, centrifugally. Phellem cells of flooded plants just differentiated from the phellogen had dense cytoplasm and rounded nuclei with a more or less central position; those further away from the phellogen showed sparse cytoplasm and their nuclei were pulled towards either tip of the cells or laid against the cell walls.
Growth in stagnant, oxygen-deficient nutrient solution increased porosity in adventitious roots of two monocotyledonous (Carex acuta and Juncus effusus) and three dicotyledonous species (Caltha palustris, Ranunculus sceleratus and Rumex palustris) wetland species from 10 to 30% under aerated conditions to 20–45%. The spatial patterns of radial oxygen loss (ROL), determined with root-sleeving oxygen electrodes, indicated a strong constitutive ‘barrier’ to ROL in the basal root zones of the two monocotyledonous species. In contrast, roots of the dicotyledonous species showed no significant ‘barrier’ to ROL when grown in aerated solution, and only a partial ‘barrier’ when grown in stagnant conditions. This partial ‘barrier’ was strongest in C. palustris, so that ROL from basal zones of roots of R. sceleratus and R. palustris was substantial when compared to the monocotyledonous species. ROL from the basal zones would decrease longitudinal diffusion of oxygen to the root apex, and therefore limit the maximum penetration depth of these roots into anaerobic soil. Further studies of a larger number of dicotyledonous wetland species from a range of substrates are required to elucidate the ecophysiological consequences of developing a partial, rather than a strong, ‘barrier’ to ROL.