Ontogeny and distribution of cell‐wall glycans during aerenchyma formation in roots of Pistia stratiotes (Araceae)

Aerenchyma is widely known to be lysigenous, schizogenous or, more recently, expansigenous. The interpretation and understanding of its function is questionable, given the lack of extensive knowledge on the development and cellular changes of this tissue. The aerenchyma of Pistia stratiotes roots reportedly originates from packet lysigeny. However, our observations suggest schizogenous development. Our objective was to analyse ontogeny of aerenchyma in P. stratiotes roots and evaluate the morphological and chemical changes in the cell wall during the formation of aerenchyma. The aerenchymatous inner cortex of schizogenous origin was observed under light and electron microscopy. Lacunae are formed by the separation, division and stretching of cells, which remain alive until maturity. Analyses using monoclonal anti‐glycan antibodies show that formation of that type of aerenchyma apparently proceeds through the same mechanisms as the genesis of intercellular spaces. However, the greatest changes occur when cells undergo stretching, including the loss of methyl‐esterification and detection of arabinans, which are not directly involved in cell separation. Thus, other factors may account for the formation of schizogenous aerenchyma.     

植物根内通气组织形成的研究进展

植物能否在湿地或淹涝环境中生长,很大程度上取决于植物是否具有健全发达的通气组织。在结合形态学和分子生物学等方面研究的基础上,概述了植物根内通气组织的形成过程,主要涉及生理功能、诱导因子和相关酶等,推测细胞程序性死亡是溶生性通气组织形成的机理,乙烯在整体信号转导网络中起关键性中介作用。     

Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence

Abstract: Enhanced development of gas-spaces beyond that due to the partial cell separation normally found in ground parenchymas and their derivatives creates tissue commonly termed "aerenchyma". Aerenchyma can substantially reduce internal impedance to transport of oxygen, nitrogen and various metabolically generated gases such as carbon dioxide and ethylene, especially between roots and shoots. Such transport lessens the risk of asphyxiation under soil flooding or more complete plant submergence, and promotes radial oxygen loss from roots leading to oxidative detoxification of the rhizo-sphere. Aerenchyma can also increase methane loss from waterlogged sediments via plants to the atmosphere. This review of the formation and functioning of aerenchyma particularly emphasises research findings since 1992 and highlights prospects for the future. Regarding formation, attention is drawn to how little is known of the regulation and processes that create schizogenous aerenchyma with its complex cell arrangements and differential cell to cell adhesion. More progress has been made in understanding lysigenous aerenchyma development. The review highlights recent work on the processes that sense oxygen deficiency and ethylene signals, subsequent transduction processes which initiate cell death, and steps in protoplast and wall degeneration that create the intercellular voids. Similarities between the programmed cell death and its causes in animals and the predictable patterns of cell death that create lysigenous aerenchyma are explored. Recent findings concerning function are addressed in terms of the diffusion aeration of roots, rhizosphere oxygenation and sediment biogeochemistry, photosynthesis and ventilation, pressurised gas-flows and greenhouse gas emissions and aspects of ventilation related to secondary thickening.     

Ethylene‐dependent aerenchyma formation in adventitious roots is regulated differently in rice and maize

In roots of gramineous plants, lysigenous aerenchyma is created by the death and lysis of cortical cells. Rice (Oryza sativa) constitutively forms aerenchyma under aerobic conditions, and its formation is further induced under oxygen‐deficient conditions. However, maize (Zea mays) develops aerenchyma only under oxygen‐deficient conditions. Ethylene is involved in lysigenous aerenchyma formation. Here, we investigated how ethylene‐dependent aerenchyma formation is differently regulated between rice and maize. For this purpose, in rice, we used the reduced culm number1 (rcn1) mutant, in which ethylene biosynthesis is suppressed. Ethylene is converted from 1‐aminocyclopropane‐1‐carboxylic acid (ACC) by the action of ACC oxidase (ACO). We found that OsACO5 was highly expressed in the wild type, but not in rcn1, under aerobic conditions, suggesting that OsACO5 contributes to aerenchyma formation in aerated rice roots. By contrast, the ACO genes in maize roots were weakly expressed under aerobic conditions, and thus ACC treatment did not effectively induce ethylene production or aerenchyma formation, unlike in rice. Aerenchyma formation in rice roots after the initiation of oxygen‐deficient conditions was faster and greater than that in maize. These results suggest that the difference in aerenchyma formation in rice and maize is due to their different mechanisms for regulating ethylene biosynthesis.     

Distinct mechanisms for aerenchyma formation in leaf sheaths of rice genotypes displaying a quiescence or escape strategy for flooding tolerance

Background and Aims

Rice is one of the few crops able to withstand periods of partial or even complete submergence. One of the adaptive traits of rice is the constitutive presence and further development of aerenchyma which enables oxygen to be transported to submerged organs. The development of lysigenous aerenchyma is promoted by ethylene accumulating within the submerged plant tissues, although other signalling mechanisms may also co-exist. In this study, aerenchyma development was analysed in two rice (Oryza sativa) varieties, ‘FR13A’ and ‘Arborio Precoce’, which show opposite traits in flooding response in terms of internode elongation and survival.

Methods

The growth and survival of rice varieties under submergence was investigated in the leaf sheath of ‘FR13A’ and ‘Arborio Precoce’. The possible involvement of ethylene and reactive oxygen species (ROS) was evaluated in relation to aerenchyma formation. Cell viability and DNA fragmentation were determined by FDA/FM4-64 staining and TUNEL assay, respectively. Ethylene production was monitored by gas chromatography and by analysing ACO gene expression. ROS production was measured by using Amplex Red assay kit and the fluorescent dye DCFH₂-DA. The expression of APX1 was also evaluated. AVG and DPI solutions were used to test the effect of inhibiting ethylene biosynthesis and ROS production, respectively.

Key Results

Both the varieties displayed constitutive lysigenous aerenchyma formation, which was further enhanced when submerged. ‘Arborio Precoce’, which is characterized by fast elongation when submerged, showed active ethylene biosynthetic machinery associated with increased aerenchymatous areas. ‘FR13A’, which harbours the Sub1A gene that limits growth during oxygen deprivation, did not show any increase in ethylene production after submersion but still displayed increased aerenchyma. Hydrogen peroxide levels increased in ‘FR13A’ but not in ‘Arborio Precoce’.

Conclusions

While ethylene controls aerenchyma formation in the fast-elongating ‘Arborio Precoce’ variety, in ‘FR13A’ ROS accumulation plays an important role.     

Nitric oxide is essential for the development of aerenchyma in wheat roots under hypoxic stress

In response to flooding/waterlogging, plants develop various anatomical changes including the formation of lysigenous aerenchyma for the delivery of oxygen to roots. Under hypoxia, plants produce high levels of nitric oxide (NO) but the role of this molecule in plant‐adaptive response to hypoxia is not known. Here, we investigated whether ethylene‐induced aerenchyma requires hypoxia‐induced NO. Under hypoxic conditions, wheat roots produced NO apparently via nitrate reductase and scavenging of NO led to a marked reduction in aerenchyma formation. Interestingly, we found that hypoxically induced NO is important for induction of the ethylene biosynthetic genes encoding ACC synthase and ACC oxidase. Hypoxia‐induced NO accelerated production of reactive oxygen species, lipid peroxidation, and protein tyrosine nitration. Other events related to cell death such as increased conductivity, increased cellulase activity, DNA fragmentation, and cytoplasmic streaming occurred under hypoxia, and opposing effects were observed by scavenging NO. The NO scavenger cPTIO (2‐(4‐carboxyphenyl)‐4,4,5,5‐tetramethylimidazoline‐1‐oxyl‐3‐oxide potassium salt) and ethylene biosynthetic inhibitor CoCl₂ both led to reduced induction of genes involved in signal transduction such as phospholipase C, G protein alpha subunit, calcium‐dependent protein kinase family genes CDPK, CDPK2, CDPK 4, Ca‐CAMK, inositol 1,4,5‐trisphosphate 5‐phosphatase 1, and protein kinase suggesting that hypoxically induced NO is essential for the development of aerenchyma.     

Aerenchyma develops by cell lysis in roots AND CELL SEPARATION IN LEAF PETIOLES IN Sagittaria lancifolia (Alismataceae)

Aerenchyma gas spaces are important for plants that survive flooding because these spaces provide an internal pathway for oxygen transport to the root zone. The objective of this study was to characterize the development of aerenchyma gas spaces in Sagittaria lancifolia L., a dominant species in freshwater wetlands adjacent to the Gulf of Mexico. Tissue at different developmental stages was collected from hydroponically grown plants, embedded in plastic, and sections were observed with a light microscope. In S. lancifolia roots, lysigeny (cell lysis) produced gas spaces that increased in volume from the root meristem to the most mature root tissue. Shoot aerenchyma occurred in the large petioles of S. lancifolia and through the blade midrib, but not in the laminar portion of the blade. In contrast to the roots, gas spaces in the petiole were formed by schizogeny (cell separation during development). Shoot initials produced cells that formed interlocking cylinders in the cortex and diaphragm cells that bridged the central portion of the cylinders. Division and expansion of both these cell types increased the diameter of the cylinders and created schizogenous gaps between diaphragm layers that produced large gas spaces in mature tissue. Therefore, aerenchyma development occurs by two different processes in S. lancifolia.     

Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil

Background and Aims

Aerenchyma provides a low-resistance O₂ transport pathway that enhances plant survival during soil flooding. When in flooded soil, soybean produces aerenchyma and hypertrophic stem lenticels. The aims of this study were to investigate O₂ dynamics in stem aerenchyma and evaluate O₂ supply via stem lenticels to the roots of soybean during soil flooding.

Methods

Oxygen dynamics in aerenchymatous stems were investigated using Clark-type O₂ microelectrodes, and O₂ transport to roots was evaluated using stable-isotope ¹⁸O₂ as a tracer, for plants with shoots in air and roots in flooded sand or soil. Short-term experiments also assessed venting of CO₂ via the stem lenticels.

Key Results

The radial distribution of the O₂ partial pressure (pO₂) was stable at 17 kPa in the stem aerenchyma 15 mm below the water level, but rapidly declined to 8 kPa at 200–300 µm inside the stele. Complete submergence of the hypertrophic lenticels at the stem base, with the remainder of the shoot still in air, resulted in gradual declines in pO₂ in stem aerenchyma from 17·5 to 7·6 kPa at 13 mm below the water level, and from 14·7 to 6·1 kPa at 51 mm below the water level. Subsequently, re-exposure of the lenticels to air caused pO₂ to increase again to 14–17 kPa at both positions within 10 min. After introducing ¹⁸O₂ gas via the stem lenticels, significant ¹⁸O₂ enrichment in water extracted from roots after 3 h was confirmed, suggesting that transported O₂ sustained root respiration. In contrast, slight ¹⁸O₂ enrichment was detected 3 h after treatment of stems that lacked aerenchyma and lenticels. Moreover, aerenchyma accelerated venting of CO₂ from submerged tissues to the atmosphere.

Conclusions

Hypertrophic lenticels on the stem of soybean, just above the water surface, are entry points for O₂, and these connect to aerenchyma and enable O₂ transport into roots in flooded soil. Stems that develop aerenchyma thus serve as a ‘snorkel’ that enables O₂ movement from air to the submerged roots.     

Cortical development in roots of the aquatic plant Pontederia cordata (Pontederiaceae)

Adventitious roots of marsh-grown Pontederia cordata were examined to determine cortical development and structure. The innermost layer of the ground meristem forms the endodermis and aerenchymatous cortex. The outermost layer of the early ground meristem undergoes a precise pattern of oblique and periclinal cell divisions to produce a single or double layer of prohypodermis with an anchor cell for each radial file of aerenchyma cells. At maturity, endodermal cell walls are modified only by narrow Casparian bands. The central regions of the ground meristem become proaerenchyma and exhibit asymmetric cell division and expansion. They produce an aerenchymatous zone with barrel-shaped large cells and irregularly shaped small cells traversing the aerenchyma horizontally along radii; some crystalliferous cells with raphides are present in the aerenchyma. The walls of the hypodermis are modified early by polyphenols. The outermost layer of the hypodermis later matures into an exodermis with Casparian bands that are impermeable to berberine, an apoplastic tracer dye. The nonexodermal layer(s) of the hypodermis has suberin-modified walls. Radial files of aerenchyma are usually connected by narrow protuberances near their midpoints, the aerenchyma lacunae having been produced by expansion of cells along walls lining intercellular spaces. We are terming this type of aerenchyma development, which is neither schizogenous nor lysigenous, "differential expansion."     

Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1

Aerenchyma tissues form gas-conducting tubes that provide roots with oxygen under hypoxic conditions. Although aerenchyma have received considerable attention in Zea mays, the signaling events and genes controlling aerenchyma induction remain elusive. Here, we show that Arabidopsis thaliana hypocotyls form lysigenous aerenchyma in response to hypoxia and that this process involves H(2)O(2) and ethylene signaling. By studying Arabidopsis mutants that are deregulated for excess light acclimation, cell death, and defense responses, we find that the formation of lysigenous aerenchyma depends on the plant defense regulators LESION SIMULATING DISEASE1 (LSD1), ENHANCED DISEASE SUSCEPIBILITY1 (EDS1), and PHYTOALEXIN DEFICIENT4 (PAD4) that operate upstream of ethylene and reactive oxygen species production. The obtained results indicate that programmed cell death of lysigenous aerenchyma in hypocotyls occurs in a similar but independent manner from the foliar programmed cell death. Thus, the induction of aerenchyma is subject to a genetic and tissue-specific program. The data lead us to conclude that the balanced activities of LSD1, EDS1, and PAD4 regulate lysigenous aerenchyma formation in response to hypoxia.     

Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species

To adapt to waterlogging, maize (Zea mays) forms lysigenous aerenchyma in root cortex as a result of ethylene-promoted programmed cell death (PCD). Respiratory burst oxidase homolog (RBOH) gene encodes a homolog of gp91^phox in NADPH oxidase, and has a role in the generation of reactive oxygen species (ROS). Recently, we found that during aerenchyma formation, RBOH was upregulated in all maize root tissues examined, whereas an ROS scavengingrelated metallothionein (MT) gene was downregulated specifically in cortical cells. Together these changes should lead to high accumulations of ROS in root cortex, thereby inducing PCD for aerenchyma formation. As further evidence of the involvement of ROS in root aerenchyma formation, the PCD was inhibited by diphenyleneiodonium (DPI), an NADPH oxidase inhibitor. Based on these results, we propose a model of cortical cell-specific PCD for root aerenchyma formation.Key words: aerenchyma, ethylene, laser microdissection, maize (Zea mays), metallothionein, programmed cell death, reactive oxygen species, respiratory burst oxidase homologIn both wetland and non-wetland plants, lysigenous aerenchyma is formed in roots by creating gas spaces as a result of death and subsequent lysis of some cortical cells, and allows internal transport of oxygen from shoots to roots under waterlogged soil conditions.^1–3 In rice (Oryza sativa) and some other wetland plant species, lysigenous aerenchyma is constitutively formed under aerobic conditions, and is further enhanced under waterlogged conditions.⁴ On the other hand, in non-wetland plants, including maize (Zea mays), lysigenous aerenchyma does not normally form under well-drained soil conditions, but is induced by waterlogging.⁵ Ethylene is involved in lysigenous aerenchyma formation,^1–3,6,7 but the molecular mechanisms are unclear.We recently identified two reactive oxygen species (ROS)-related genes that were specifically regulated in maize root cortex by waterlogged conditions, but not in the presence of an ethylene perception inhibitor 1-methylcyclopropene (1-MCP).⁵ One was respiratory burst oxidase homolog (RBOH), which has a role in ROS generation and the other was metallothionein (MT), which has a role in ROS scavenging. These results suggest that ROS has a role in ethylene signaling in the PCD that occurs during lysigenous aerenchyma formation.     

Oligochitosan induces programmed cell death in tobacco suspension cells

Oligochitosan has been proved to trigger plant cell death. To gain some insights into the mechanisms of oligochitosan-induced cell death, the nature of oligochitosan-induced cell death and the role of calcium (Ca²⁺), nitric oxide (NO) and hydrogen peroxide (H₂O₂) were studied in tobacco suspension cells. Oligochitosan-induced cell death occurred in cytoplasmic shrinkage, phosphatidylserine externalization, chromatin condensation, TUNEL-positive nuclei, cytochrome c release and induction of programmed cell death (PCD)-related gene hsr203J, suggesting the activation of PCD pathway. Pretreatment cells with cyclosporin A, resulted in reducing oligochitosan-induced cytochrome c release and cell death, indicating oligochitosan-induced PCD was mediated by cytochrome c. In the early stage, cells undergoing PCD showed an immediate burst in free cytosolic Ca²⁺ ([Ca²⁺]_cyt) elevation, NO and H₂O₂ production. Further study showed that these three signals were involved in oligochitosan-induced PCD, while Ca²⁺ and NO played a negative role in this process by modulating cytochrome c release.     

Changes in cell structure during the formation of root aerenchyma inSAGITTARIA LANCIFOLIA (Alismataceae)

In many wetland species, root aerenchyma is produced by the predictable collapse of root cortex cells, indicating a programmed cell death (PCD). The objective of this study was to characterize the cellular changes that accompany this PCD in the marsh species Sagittaria lancifolia. Structural changes in membranes and organelles were examined during development of root cortex cells to compare with previous examples of PCD. The organization of cortical microtubule (CMT) arrays in root cells from S. lancifolia was also evaluated as a possible predictor of cell lysis. Nuclear fragmentation and condensation were the earliest changes observed in cells undergoing lysis. Breakdown of the tonoplast and other organelles and disruption of the plasma membrane followed. After loss of cytoplasm, cells collapsed to form gas spaces. These results were compared to collapse of root cortical cells of Zea mays and Oryza sativa during aerenchyma development. Changes in the appearance of the cytoplasm of all three species were similar at later stages of aerenchyma development. The relative timing of disintegration of the tonoplast and middle lamella appeared to differ among the three species. Changes in the organization of CMT arrays did not appear to be a predictor of PCD in S. lancifolia. Aerenchyma production in plants involves a type of PCD that is morphologically distinct from PCD described from many animals.     

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.     

AERENCHYMA DEVELOPMENT IN WATERLOGGED PLANTS

Aerenchyma development in waterlogged Helianthus annuus, Lycopersicon esculentum, and Salix fragilis was studied. More than half of the root cortical tissue sometimes became an air cavity in willow roots which developed in water. There was no cortical aerenchyma in the terminal portion, but more advanced aerenchyma developed towards the base of the sunflower roots formed in water. Waterlogged sunflower and tomato plants developed lysigenous aerenchyma in the cortex of waterlogged stems within two days.     

Gas space and oxygen exchange in roots of Avicennia marina (Forssk.) Vierh. var. australasica (Walp.) Moldenke ex N. C. Duke,the Grey Mangrove

Aerenchyma pervades the cortex of the whole root system in Avicenniamarina var. australasica plants grown for 3 to 5 years in artificial-tidaltanks. The gas spaces appear to be schizogenous in all but the finest roots,where some apparently lysigenous gas spaces develop. Gas spaces in thepith are small. Pneumatophores examined at the time the tips are growingpossess subrisules on the tips as well as lenticels on mature regions. At othertimes subrisules are not seen. When the tide floods the pneumatophores,gas pressure and oxygen concentration go down – pressure by 1.7 kPa orless, but oxygen by as much as 3 mol m^-3, or more in some cases.On draining, pressure recovers immediately to atmospheric, but oxygenslowly rises to a plateau below the concentration in the atmosphere. Thechanges in oxygen concentration are consistent with oxygen supply bydiffusion. The contribution of oxygen made by the small influx of air onpressure recovery is only a minor fraction of the respiratory oxygenrequirement. Wet weather at low tide restricts gas exchange, affecting bothpressure and oxygen. The pressure and oxygen changes are repeated overmany tidal cycles. The results are compared with those for other speciesand situations in the literature.     

1-Butanol triggers programmed cell death in Populus euphratica cell cultures

1-Butanol, which is a specific inhibitor of phospholipase D, usually inhibits phosphatidic acid (PA) production and blocks the PA-dependent signaling pathway under stress conditions. However, the effects of 1-butanol on plant cells under non-stress condition are still unclear. In this study, we report that 1-butanol induced a dose dependent cell death in poplar (Populus euphratica) cell cultures. In contrast, the control 2-butanol and ethanol had no effects on cell viability. 1-Butanol-treated cells displayed hallmark features of programmed cell death (PCD), such as shrinkage of the cytoplasm, DNA fragmentation, condensed or stretched chromatin and the activation of caspase-3-like protease. Exogenous application of PA markedly inhibited the 1-butanol-induced PCD. 1-Butanol also caused a burst of mitochondrial H₂O₂ ([H₂O₂]_mit) that was usually accompanied by a loss of mitochondrial membrane potential (?Ψm). Supplement of PA, antioxidant enzyme (catalase) and antioxidant (ascorbic acid) reversed this effect. Moreover, a significant increase of nitric oxide (NO) was observed in 1-butanol-treated poplar cells. This NO burst was suppressed by PA or inhibitors of NO synthesis. Further pharmacological experiments indicate that the burst of NO contributed to the 1-butanol-induced inhibition of antioxidant enzymes and subsequent H₂O₂-dependent PCD. In conclusion, we propose that 1-butanol is a potent inducer of PCD in plants and this process is regulated by the PA, NO and H₂O₂.     

Cell death induced by ozone stress in the leaves of Populus deltoides × maximowiczii

When exposed to an acute ozone stress, cell death occurred in leaves of the O₃ sensitive Populus deltoides × maximowiczii clone Eridano. After treatment (5 h fumigation and 24 h recovery), the damaged areas covered more than 50 % of the leaf surface. At cellular level, these lesions were preceded by some apoptotic hallmarks and by biochemical and physiological alterations evoked by the apoplastic O₃ dissociation. The cell death pattern was highly localized and involved an increase of membrane permeability, externalization of phosphatidylserine, DNA fragmentation, callose accumulation, polyphenol production, and a biphasic oxidative burst accompanied by NO overproduction. These results indicate a process of programmed cell death that could have the biological significance of limiting the spreading the oxidative burst triggered by ozone dissociation in apoplastic environment. Moreover, materials derived from cell dismantling could be remobilized toward developing structures which can conclude their ontogenetic program after the stress.     

Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species

The root anatomical features of eight mangrove species in Hong Kong were similar, with large aerenchymal lacunae in the cortex for efficient internal oxygen transfer and an outer barrier consisting of an epidermis and hypodermis to prevent oxygen loss. The spatial pattern of radial oxygen loss (ROL) was also comparable, with more oxygen lost from the tip than that from the basal and mature zones. However, the aerenchyma in the cortex, the barrier and the extent of ROL varied along the root and these variations were species-specific. The whole root of Avicennia marina (Forsk.) Vierh., Acanthus ilicifolius L., Aegiceras corniculatum (Linn.) Blanco, Kandelia obovata Sheue, Liu & Yong (previously known as Kandelia candel (L.) Druce) and Heriteria littoralis Dryand. ex W. Ait. had schizogenous aerenchyma, while the aerenchyma of Lumnitzera racemosa Willd. and Bruguiera gymnorrhiza (L.) Poir changed from schizogenous in the root tip to lysigenous in the other parts of the root. Excoecaria agallocha L. displayed the opposite pattern, from lysigenous in the root tip to schizogenous further up. Among the eight species, the roots of A. marina and A. ilicifolius had the largest areas of aerenchyma air spaces, but they also had the weakest barrier. On the other hand, H. littoralis had the least longitudinal oxygen transfer because of its smaller area of aerenchyma air spaces in its root. The tolerance of mangrove species to waterlogged soil followed the order of A. marina (most foreshore species) > A. ilicifolius > K. obovata > A. corniculatum > B. gymnorrhiza > E. agallocha > L. racemosa > H. littoralis (most landward species), which is related to their anatomical features of root cortex, epidermis and hypodermis.