Development Of Aerenchyma In Roots Research Articles

Physiological, Cellular, and Transcriptomic Analyses Provide Insights into the Tolerance Response of Arundo donax to Waterlogging Stress

Arundo donax is widely used as an ornamental plant in landscape gardening because of its adaptability to varying degrees of waterlogged conditions. However, to date, little information is available about the adaptive mechanism of A. donax under waterlogging stress. The results showed that long-term mild waterlogging efficiently induced the formation of adventitious roots (ARs) and further promoted root aerenchyma development, and that the activity of antioxidant enzymes (SOD, POD, and CAT) in Ars also was greatly enhanced after waterlogging. At the transcriptomic level, the expression of genes related to apoptosis, the regulation of cell division, ethylene biosynthesis, alginate synthesis, auxin signaling pathways, and anaerobic respiration was mostly up-regulated after the occurrence of waterlogging stress but genes involved in the abscisic acid signaling pathways were partly down-regulated, which indicated a preferential and favorable transcriptional response in regulating adventitious root development. Taken together, this study definitely advances our knowledge of the morphological, physiological, and transcriptomic responses of A. donax under waterlogging stress and sheds new lights on its adaptive mechanisms.

Effects of plant physiological responses under nitrogen stress on pollutant removal in subsurface constructed wetlands

Nitrogen loading directly affects plant metabolism, morphogenesis and rhizosphere effect, and then the pollutant removal performance of constructed wetlands. However, the nitrogen loading standards are significantly different in many design specifications around the world. The physiological responses of plants (Canna indica) and pollutant removal characteristics under different nitrogen stresses (NSs) in subsurface flow constructed wetlands (SFCWs) were investigated. Under appropriate NS of 120 mgN/L, the enhancement of stress resistance and the stabilization of cell structures of Canna indica were sustainable. However, with excessive NSs of 0, 300 and 600 mgN/L, the cell structure was damaged permanently. Appropriate NS could significantly increase the radial oxygen loss and dissolved oxygen concentration in SFCWs by 40.33 % and 43.11 % by persistently enhancing oxygen production (photosynthesis) and delivery capacity (root aerenchyma development) (p < 0.01). Simultaneously, the abundance and diversity of nitrogen-transforming bacteria significantly increased (p < 0.01), the activities of ammonia monooxygenase, periplasmic nitrate reductase and the removal rate of NH4+ − N and NO3− − N almost doubled. Controlling nitrogen loading is very important since NS would lead to the organic and irreversible difference in aerenchyma development in roots throughout the whole growth period of plants, which could persistently affect the removal efficiency and stability of pollutants in SFCWs.

Newly identified miRNAs may contribute to aerenchyma formation in sugarcane roots.

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.

Relationship between Root Aeration and Oil Tolerance in Four Wetland Species

Plant physiological tolerance to oil exposure has been linked to flooding tolerance, as both conditions induce anoxic conditions in the soil. It was hypothesized that tolerance of wetland plants to oil was due to enhanced development of root aerenchyma, which could aerate submerged tissues and support aerobic respiration during anoxic conditions resulting from oil exposure. In this study, four wetland grasses of varying tolerance to anoxic conditions were subjected to 6 L m-2 motor oil in greenhouse experiments for six weeks and root aerenchyma was assessed by microscopy. Physiological tolerance to spilled oil came from an ability to supply oxygen internally to submerged tissues and to anatomical barrier layers that maintain integrity of root structure. The most oil tolerant species, Phragmites australis (common reed) and Spartina alterniflora (smooth cordgrass), had extensive root aerenchyma, which could ventilate oil-coated roots and support aerobic respiration. Moderate oil tolerance was observed in Spartina pectinata (prairie cordgrass), which was supported by root aerenchyma development, but with minor damage in structure under oil-impacted conditions. The most sensitive species to oil, Phalaris arundinacea (reed canarygrass), had less aerenchyma in roots and extensive root damage from oil exposure. Complete degradation of the root cortex was observed in Phalaris arundinacea and, therefore, a reduction in aerenchyma. These data help explain physiological differences among species exposed to spilled oil. Root aerenchyma provides aeration to support respiration in oiled roots, and an effective barrier at the exodermis helps to maintain root cortical structure.

Waterlogging tolerance is associated with root porosity in barley (Hordeum vulgare L.)

Tolerance to waterlogging is an important breeding objective for barley (Hordeum vulgare L.); however, it is a complex quantitative trait. It is difficult to screen large numbers of lines in the field due to environmental variability, and it is also challenging to screen large numbers in controlled conditions if yield data are to be collected. The direct measurement of traits that contribute to waterlogging tolerance, such as aerenchyma development in roots, may offer advantages especially if molecular markers can be developed to screen breeding populations. A doubled haploid population from a cross between Franklin and YuYaoXiangTian Erleng was screened for adventitious root porosity (gas-filled volume per unit root volume) as an indicator of aerenchyma formation. A single QTL for root porosity was identified on chromosome 4H which explained 35.7 and 39.0 % of phenotypic variation in aerated and oxygen-deficient conditions, respectively. The nearest marker was EBmac0701. This QTL is located in the same chromosomal region that contributed to tolerance when the same population was screened in an earlier independent soil waterlogging experiment. Comparative mapping revealed that this QTL is syntenic with the Qaer1.02-3 QTL in maize and the Sub1A-1 gene in rice, which are associated with aerenchyma formation (maize) and submergence tolerance (rice), respectively. This is the first report of a QTL for root porosity in barley which elucidates a major mechanism of waterlogging tolerance.

Roles of Root Aerenchyma Development and Its Associated QTL in Dry Matter Production under Transient Moisture Stress in Rice

Enhanced aerenchyma development in rice under transient drought-to-waterlogged (TD-W) stress promotes root system development by promoting lateral root production. This study analyzed the quantitative trait loci (QTLs) associated with the plasticity in aerenchyma development under TD-W stress. A mapping population of 60 F2 genotypes of chromosome segment substituted lines (CSSL) derived from CSSL47 and Nipponbare crosses were grown in rootboxes and evaluated for shoot and root growth, and aerenchyma development (expressed as root porosity). The TD-W stress was imposed starting with water saturated soil condition at sowing and then to progressive drought from 0 to 21 days after sowing (DAS) prior to exposure to sudden waterlogging for another 17 days (21 to 38 DAS). We performed simple and composite interval mapping to identify QTLs for aerenchyma development. QTL associated with aerenchyma development was mapped on the short-arm of chromosome 12 and designated as qAER-12. The effect of qAER-12 on the plasticity in aerenchyma development under TD-W was significantly associated with the increase in lateral root elongation and branching. This resulted in greater root system development as expressed in total root length and consequently contributed to higher dry matter production. This qAER-12 is probably the first reported QTL associated with aerenchyma development in rice under TD-W and is a useful trait for the improvement of the adaptive capability under fluctuating soil moisture conditions.

Root and leaf changes in Salix nigra cuttings in response to increasing soil temperature

Salix nigra, black willow, is used for wetland restoration and streambank stabilization and like other wetland species has the ability to develop aerenchyma tissue to avoid root anoxia. Root aerenchyma development could be affected if the temperature of the rhizosphere increases as a result of climatic change. Root porosity (used as an indication of aerenchyma tissue) of S. nigracuttings grown under three soil temperature regimes was found to increase in response to increases in temperature (F2,40 = 56.57; p < 0.0001). There was also an increase in internal C (carbon) concentration (F2,27 = 27.36; P < 0.0001) and a corresponding decrease in stomatal conductance (F2,27 = 3.728; P = 0.037), transpiration rate (F2,27 = 5.084; P = 0.013), and net photosynthesis (F2,27 = 14.07; P < 0.0001) in response to increased soil temperature. The present research demonstrated that the stress response of S. nigra to increased soil temperature is similar to its response to anoxic conditions. Key words: Aerenchyma, global warming, Salix nigra, remediation, rhizospere, riparian systems.

Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots

In waterlogged soil, deficiency of oxygen triggers development of aerenchyma in roots which facilitates gas diffusion between roots and the aerial environment. However, in contrast to other monocots, roots of rice (Oryza sativa L.) constitutively form aerenchyma even in aerobic conditions. The formation of cortical aerenchyma in roots is thought to occur by either lysigeny or schizogeny. Schizogenous aerenchyma is developed without cortical cell death. However, lysigenous gas-spaces are formed as a consequence of senescence of specific cells in primary cortex followed by their death due to autolysis. In the last stage of aerenchyma formation, a 'spoked wheel' arrangement is observed in the cortical region of root. Ultrastructural studies show that cell death is constitutive and no characteristic cell structural differentiation takes place in the dying cells with respect to surrounding cells. Cell collapse initiation occurs in the center of the cortical tissues which are characterized by shorter with radically enlarged diameter. Then, cell death proceeds by acidification of cytoplasm followed by rupturing of plasma membrane, loss of cellular contents and cell wall degradation, while cells nuclei remain intact. Dying cells releases a signal through symplast which initiates cell death in neighboring cells. During early stages, middle lamella-degenerating enzymes are synthesized in the rough endoplasmic reticulum which are transported through dictyosome and discharged through plasmalemma beneath the cell wall. In rice several features of root aerenchyma formation are analogous to a gene regulated developmental process called programmed cell death (PCD), for instance, specific cortical cell death, obligate production of aerenchyma under environmental stresses and early changes in nuclear structure which includes clumping of chromatin, fragmentation, disruption of nuclear membrane and apparent engulfment by the vacuole. These processes are followed by crenulation of plasma membrane, formation of electron-lucent regions in the cytoplasm, tonoplast disintegration, organellar swelling and disruption, loss of cytoplasmic contents, and collapse of cell. Many processes in lysing cells are structural features of apoptosis, but certain characteristics of apoptosis i.e., pycnosis of the nucleus, plasma membrane blebbing, and apoptotic bodies formation are still lacking and thus classified as non-apoptotic PCD. This review article, describes most recent observations alike to PCD involved in aerenchyma formation and their systematic distributions in rice roots.

Root growth, aerenchyma development, and oxygen transport in rice genotypes subjected to drought and waterlogging

Soils under field conditions may experience fluctuating soil water regimes ranging from drought to waterlogging. The inability of roots to acclimate to such changes in soil water regimes may result in reduced growth and function thereby, dry matter production. This study compared the root and shoot growth, root aerenchyma development, and associated root oxygen transport of aerobic and irrigated lowland rice genotypes grown under well-watered (control), waterlogged, and droughted soil conditions for 30 days. The aerobic genotypes were as tolerant as the irrigated lowland genotypes under waterlogging because of their comparable abilities to enhance aerenchyma that effectively facilitated O 2 diffusion to the roots for maintaining root growth and dry matter production. Under drought, aerobic genotypes were more tolerant than the irrigated lowland genotypes due to their higher ability to maintain nodal root production, elongation, and branching, thus, less reduction in dry matter production. Aerenchyma was also formed in droughted roots regardless of genotypes, but was resistant to internal O 2 transport under O 2 deficiency. The ability of roots to resist temporal variations in drought and waterlogging stresses might have strong implications for the adaptation of rice growing in environments with fluctuating soil water regimes.

A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma.

We review literature and present new observations on the differences among three general patterns of aerenchyma origin and their systematic distributions among the flowering plants, and we clarify terminology on root aerenchyma. From our own previous works and some new observations, we have analysed the root cortex in 85 species of 41 families in 21 orders of flowering plants that typically grow in wetlands to determine the characteristic patterns of aerenchyma. A developmental and structural pattern that we term expansigeny, as manifested by honeycomb aerenchyma, is characteristic of all aquatic basal angiosperms (the Nymphaeales) and basal monocots (the Acorales). Expansigenous aerenchyma develops by expansion of intercellular spaces into lacunae by cell division and cell expansion. Schizogeny and lysigeny, so often characterized in recent reviews as the only patterns of root cortex lacunar formation, are present in most wetland plants, but are clearly not present in the most basal flowering plants. We conclude that expansigeny is the basic type of aerenchyma development in roots of flowering plants and that the presence of expansigenous honeycomb aerenchyma in root cortices was fundamental to the success of the earliest flowering plants found in wetland environments.

Transduction of an Ethylene Signal Is Required for Cell Death and Lysis in the Root Cortex of Maize during Aerenchyma Formation Induced by Hypoxia.

Ethylene has been implicated in signaling cell death in the lysigenous formation of gas spaces (aerenchyma) in the cortex of adventitious roots of maize (Zea mays) subjected to hypoxia. Various antagonists that are known to modify particular steps in signal transduction in other plant systems were applied at low concentrations to normoxic and hypoxic roots of maize, and the effect on cell death (aerenchyma formation) and the increase in cellulase activity that precedes the appearance of cell degeneration were measured. Both cellulase activity and cell death were inhibited in hypoxic roots in the presence of antagonists of inositol phospholipids, Ca2+- calmodulin, and protein kinases. By contrast, there was a parallel promotion of cellulase activity and cell death in hypoxic and normoxic roots by contact with reagents that activate G-proteins, increase cytosolic Ca2+, or inhibit protein phosphatases. Most of these reagents had no effect on ethylene biosynthesis and did not arrest root extension. These results indicate that the transduction of an ethylene signal leading to an increase in intracellular Ca2+ is necessary for cell death and the resulting aerenchyma development in roots of maize subjected to hypoxia.

Root‐to‐Shoot Communication in Flooded Plants: Involvement of Abscisic Acid, Ethylene, and 1‐Aminocyclopropane‐1‐carboxylic Acid

AbstractNonhydraulic communication between roots and shoots of flooded plants is reviewed. Contrary to reports for roots of droughted plants, those of flooded tomato plants (Lycopersicon esculentum L.) did not export increased amounts of abscisic acid (ABA) to the shoots, even though stomata closed in association with increased foliar ABA, and in the absence of marked losses in leaf hydration. Flooded tomato root systems did export more of the ethylene precursor 1‐aminocyclopropane‐1‐carboxylic acid (ACC). Ethylene formed in the leaves by oxidation of the ACC to ethylene and the epinastic leaf curvatures the ethylene induced were found to be inhibited in tomato plants transformed with an antisense gene to the ethylene‐forming enzyme ACC oxidase. Our estimates of the concentration and delivery of ABA and ACC in the xylem sap as it passes into the shoot from the roots avoided artifacts associated with variable sap flow rates and temporary contamination from wounded tissue. Measurements of ethylene production by individual roots of intact seedlings of maize (Zea mays L.) by highly sensitive photoacoustic laser detection confirmed earlier work linking enhanced ethylene evolution with more extensive aerenchyma development in roots that are partially deficient in oxygen. The development of aerenchyma enhances oxygen movement from shoots to roots.

Root Aerenchyma Development in Spartina Patens in Response to Flooding

Root Aerenchyma Development in Spartina Patens in Response to Flooding

Aerenchyma and lenticel formation in pine seedlings: A possible avoidance mechanism to anaerobic growth conditions

Seedlings of pond pine (Pinus serotinaMichx.), sand pine [P. clausa(Engelm.) Sarg.], and loblolly pine (P. taedaL., wet‐site and drought‐hardy seed sources) were grown in hydroponic solution culture using a non‐circulating, continuously flowing design under anaerobic or aerobic conditions to determine whether flooding tolerance was correlated with enhanced internal root aeration. Transport of atmospheric O2from the shoot to the root of anaerobically grown loblolly and pond pine seedlings was demonstrated via rhizosphere oxidation, using both reduced indigo‐carmine solution and a polarographic, ensheathing Pt‐electrode. Stem and root collar lenticels were the major sites of atmospheric O2entry for submerged roots in these seedlings. No O2leakage was detected from roots of aerobically grown pine seedlings. Longitudinal and radial pathways for gaseous diffusion via intercellular air spaces in the pericycle and between ray parenchyma cells, respectively, were demonstrated histo‐logically in anaerobically grown loblolly and pond pines. Rhizosphere oxidation, and lenticel and aerenchyma development in roots of flood‐intolerant sand pine seedlings grown in anaerobic solutions were minimal. Only 15 days of anaerobic growth conditions were necessary to increase internal root porosities of loblolly and pond pine seedlings – although not to the extent found in seedlings treated for 30 or 75 days. Histological results indicated that root tissue in the secondary stage of growth was capable of forming intercellular air spaces, demonstrating a degree of internal plasticity – at least in the more flood‐tolerant loblolly and pond pine seedlings.

Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen

Adventitious roots of two to four-weekold intact plants of Zea mays L. (cv. LG11) were shorter but less dense after extending into stagnant, non-aerated nutrient solution than into solution continuously aerated with air. Dissolved oxygen in the non-aerated solutions decreased from 21 kPa to 3-9 kPa within 24 h. When oxygen partial pressures similar to those found in non-aerated solutions (3, 5 and 12 kPa) were applied for 7 d to root systems growing in vigorously bubbled solutions, the volume of gas-space in the cortex (aerenchyma) was increased several fold. This stimulation of aerenchyma was associated with faster ethylene production by 45-mm-long apical root segments. When ethylene production by roots exposed to 5 kPa oxygen was inhibited by aminoethoxyvinylglycine (AVG) dissolved in the nutrient solution, aerenchyma formation was also retarded. The effect of AVG was reversible by concomitant applications of 1-aminocyclopropane-1-carboxylic acid, an immediate precursor of ethylene. Addition of silver nitrate, an inhibitor of ethylene action, to the nutrient solution also prevented the development of aerenchyma in roots given 5 kPa oxygen. Treating roots with only 1 kPa oxygen stimulated ethylene production but failed to promote gas-space formation. These severely oxygen-deficient roots seemed insensitive to the ethylene produced since a supplement of exogeneous ethylene that promoted aerenchyma development in nutrient solution aerated with air (21 kPa oxygen) failed to do so in nutrient solution supplied with 1 kPa oxygen. Both ethylene production and aerenchyma formation were almost completely halted when roots were exposed to nutrient solutions devoid of oxygen. Thus both processes require oxygen and are stimulated by oxygen-deficient surroundings in the 3-to 12-kPa range of oxygen partial pressures when compared with rates observed in air (21 kPa oxygen).

Aspects of an experimental study on root aerenchyma development and the ecological implications thereof

Anaerobic conditions induced cortical aerenchyma in maize roots cultivated in water culture. Similar results were obtained by growing the plants in nitrate and phosphate deficient solutions but the cavitation was more severe when conditions were anaerobic. Low temperatures delayed the onset of these symptoms. Mineral deficiencies also regulated the formation of root hairs in water culture. In the field, the behaviour of the rooting systems in a group of Restionaceae with aerenchyma was interpreted from anatomical and developmental data.