Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere

Young Phragmites plants were grown in two cocktails of monocarboxylic acids (C(1)-C(5)) at pH 6, where the concentration of each acid was innocuous and the total undissociated (potentially toxic) concentrations were 0.35 mmol/L and 0.42 mmol/L. Rice plants were subjected to 1.5 mmol/L acetic acid at pH 4.5 (undissociated concentration = 1.05 mmol/L). In Phragmites, each cocktail curtailed root growth especially and induced premature shoot senescence. In both species, after 3-5 d of treatment, radial oxygen loss (ROL) from apical regions of adventitious roots, and from Phragmites laterals, was reduced to very low values and associated with cell wall lignification and suberization in the surface cell layers. At later stages of treatment, rice responded to acetic acid in similar ways to Phragmites, with the development of intercellular and callus type occlusions in the gas space system, vascular blockages, and the failure of laterals to emerge. The results are relevant to the supply of oxygen from Phragmites roots to sediments for the phytopurification of waste waters, to the efflux of methane and carbon dioxide from wetlands, and to rice cultivation.     

Stagnant deoxygenated growth enhances root suberization and lignifications, but differentially affects water and NaCl permeabilities in rice (Oryza sativa L.) roots

It has been shown that rice roots grown in a stagnant medium develop a tight barrier to radial oxygen loss (ROL), whereas aerated roots do not. This study investigated whether the induction of a barrier to ROL affects water and solute permeabilities. Growth in stagnant medium markedly reduced the root growth rate relative to aerated conditions. Histochemical studies revealed an early deposition of Casparian bands (CBs) and suberin lamellae (SL) in both the endodermis (EN) and exodermis, and accelerated lignification of stagnant roots. The absolute amounts of suberin, lignin and esterified aromatics (coumaric and ferulic acid) in these barriers were significantly higher in stagnant roots. However, correlative permeability studies revealed that early deposition of barriers in stagnant roots failed to reduce hydraulic conductivity (Lp(r) ) below those of aerated roots. In contrast to Lp(r) , the NaCl permeability (P(sr) ) of stagnant roots was markedly lower than that of aerated roots, as indicated by an increased reflection coefficient (σ(sr) ). In stagnant roots, P(sr) decreased by 60%, while σ(sr) increased by 55%. The stagnant medium differentially affected the Lp(r) and P(sr) of roots, which can be explained in terms of the physical properties of the molecules used and the size of the pores in the apoplast.     

The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution

The present report describes experiments in which the effects of growth in aerated and stagnant nutrient solutions on adventitious root porosities and patterns of radial O2 loss (ROL) from the roots of four genotypes of rice (Oryza sativa L.) were evaluated. The genotypes studied are usually cultivated in farming systems which differ markedly in their degree of soil waterlogging and flooding. Rice genotypes were found to differ in the constitutive porosity (% gas space) of their adventitious roots when grown in aerated solutions (lowest was 16%, highest was 30%), and the roots grown in stagnant conditions had porosities between 28% and 38%. ROL from the adventitious roots raised in aerated solution increased with distance behind the tip in three of the four genotypes; whereas for roots raised in stagnant solution, ROL decreased with distance behind the tip which is indicative of a high resistance to diffusion between the aerenchyma and external medium. For example, at 35 mm behind the root tip the ROL from roots of the 'deepwater' cultivar grown in stagnant conditions was 0.7% of the rate of its aerated roots, for the 'lowland' cultivar it was 5.6%, and for one of the 'upland' cultivars it was 43.6%. Thus, the barrier to ROL from the adventitious roots in three of the four genotypes was induced by growth in stagnant nutrient solution. A low rate of ROL from the basal zones of roots in an O2-free environment is of adaptative value since longitudinal diffusion of O2 to the root apex would be enhanced which, in turn, enables greater penetration of roots into anaerobic soils.     

Interactions among Fe2+, S2-, and Zn2+ tolerance, root anatomy, and radial oxygen loss in mangrove plants

Root anatomy, radial oxygen loss (ROL), and tolerances to ferrous (Fe(2+)), sulphide (S(2-)), and zinc (Zn(2+)) ions were investigated in seedlings of eight species of mangrove, including three pioneer species, three rhizophoraceous and two landward semi-mangrove species. The results showed an interesting co-tolerance to Fe(2+), S(2-), and Zn(2+). The three rhizophoraceous species (Bruguiera gymnorrhiza, Kandelia obovata and Rhizophora stylosa), which possessed the thickest lignified exodermis and the 'tightest barrier' in ROL spatial pattern, consistently exhibited the highest tolerance to Fe(2+), S(2-), and Zn(2+). B. gymnorrhiza could directly reduce ROL by increasing lignification within the exodermis. Such an induced barrier to ROL is a probable defence response to prevent further invasion and spread of toxins within plants. The data also indicated that, in B. gymnorrhiza, Fe(2+) or S(2-), or both, induced a lignified exodermis that delayed the entry of Zn(2+) into the roots and thereby contributed to a higher tolerance to Zn(2+). This study provides new evidence of exclusive strategies of mangrove seedling roots in dealing with contaminations. The information is also important in the selection and cultivation of tolerant species for the bioremediation of contaminated waters or soils.     

Water uptake by roots of Hordeum marinum: formation of a barrier to radial O2 loss does not affect root hydraulic conductivity

The adventitious roots of Hordeum marinum grown in stagnant deoxygenated solution contain a barrier to radial O2 loss (ROL) in basal zones, whereas roots of plants grown in aerated solution do not. The present experiments assessed whether induction of the barrier to ROL influences root hydraulic conductivity (Lpr). Wheat (Triticum aestivum) was also studied since, like H. marinum, this species forms aerenchyma in stagnant conditions, but does not form a barrier to ROL. Plants were grown in either aerated or stagnant, deoxygenated nutrient solution for 21-28 d. Root-sleeving O2 electrodes were used to assess patterns of ROL along adventitious roots, and a root-pressure probe and a pressure chamber to measure Lpr for individual adventitious roots and whole root systems, respectively. Lpr, measured under a hydrostatic pressure gradient, was 1.8-fold higher for individual roots, and 5.6-fold higher for whole roots systems, in T. aestivum than H. marinum. However, there was no difference in Lpr between the two species when measured under an osmotic driving force, when water moved from cell to cell rather than apoplastically. Root-zone O2 treatments during growth had no effect on Lpr for either species (measured in aerobic solution). It is concluded that induction of the barrier to ROL in H. marinum did not significantly affect the hydraulic conductivity of either individual adventitious roots or of the whole root system.     

Number,position, diameter and initial direction of growth of primary roots in Musa

To understand soil colonization by a root system, information is needed on the architecture of the root system. In monocotyledons, soil exploration is mainly due to the growth of adventitious primary roots. Primary root emergence in banana was quantified in relation to shoot and corm development. Root emergence kinetics were closely related to the development of aerial organs. Root position at emergence on the corm followed an asymptotic function of corm dry weight, so that the age of each root at a given time could be deduced from its position. Root diameter at emergence was related to the position of the roots on the corm, with younger roots being thicker than older ones. However, root diameters were not constant along a given root, but instead decreased with the distance to the base; roots appear to be conical in their basal and apical parts. Root growth directions at emergence were variable, but a high proportion of the primary roots emerged with a low angle to the horizontal. Further research is needed to evaluate whether these initial trajectories are conserved during root development. Results presented in this study are in good agreement with those reported for other monocotyledons such as maize and rice. They give quantitative information that will facilitate the development of models of root system architecture in banana.     

Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice

Growth of adventitious roots is induced in deepwater rice (Oryza sativa L.) when plants become submerged. Ethylene which accumulates in flooded plant parts is responsible for root growth induction. Gibberellin (GA) is ineffective on its own but acts in a synergistic manner together with ethylene to promote the number of penetrating roots and the growth rate of emerged roots. Studies with the GA biosynthesis inhibitor paclobutrazol revealed that root emergence was dependent on GA activity. Abscisic acid (ABA) acted as a competitive inhibitor of GA activity. Root growth rate on the other hand was dependent on GA concentration and ABA acted as a potent inhibitor possibly of GA but also of ethylene signaling. The results indicated that root emergence and elongation are distinct phases of adventitious root growth that are regulated through different networking between ethylene, GA and ABA signaling pathways. Adventitious root emergence must be coordinated with programmed death of epidermal cells which cover root primordia. Epidermal cell death is also controlled by ethylene, GA and ABA albeit with cell-type specific cross-talk. Different interactions between the same hormones may be a means to ensure proper timing of cell death and root emergence and to adjust the growth rate of emerged adventitious roots.     

Morphological and physiological responses of rice (Oryza sativa) to limited phosphorus supply in aerated and stagnant solution culture

BACKGROUND AND AIMS: Rain-fed lowland rice commonly encounters stresses from fluctuating water regimes and nutrient deficiency. Roots have to acquire both oxygen and nutrients under adverse conditions while also acclimating to changes in soil-water regime. This study assessed responses of rice roots to low phosphorus supply in aerated and stagnant nutrient solution. METHODS: Rice (Oryza sativa 'Amaroo') was grown in aerated solution with high P (200 micro m) for 14 d, then transferred to high or low (1.6 micro m) P supply in aerated or stagnant solution for up to 8 d. KEY RESULTS: After only 1 d in stagnant conditions, root radial oxygen loss (ROL) had decreased by 90 % in subapical zones, whereas near the tip ROL was maintained. After 4 d in stagnant conditions, maximum root length was 11 % less, and after 8 d, shoot growth was 25 % less, compared with plants in aerated solution. The plants in stagnant solution had up to 19 % more adventitious roots, 24 % greater root porosity and 26 % higher root/shoot ratio. Rice in low P supply had fewer tillers in both stagnant and aerated conditions. After 1-2 d in stagnant solution, relative P uptake declined, especially at low P supply. Aerated roots at low P supply maintained relative P uptake for 4 d, after which uptake decreased to the same levels as in stagnant solution. CONCLUSIONS: Roots responded rapidly to oxygen deficiency with decreased ROL in subapical zones within 1-2 d, indicating induction of a barrier to ROL, and these changes in ROL occurred at least 2 d before any changes in root morphology, porosity or anatomy were evident. Relative P uptake also decreased under oxygen deficiency, showing that a sudden decline in root-zone oxygen adversely affects P nutrition of rice.     

Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes

Root aeration, arsenic (As) accumulation, and speciation in rice of 20 different genotypes with regular irrigation of water containing 0.4 mg As l(-1) were investigated. Different genotypes had different root anatomy demonstrated by entire root porosity (ranging from 12.43% to 33.21%), which was significantly correlated with radial oxygen loss (ROL) (R=0.64, P<0.01). Arsenic accumulation differed between genotypes, but there were no significant differences between Indica and Japonica subspecies, as well as paddy and upland rice. Total ROL from entire roots was correlated with metal tolerance (expressed as percentage mean of control straw biomass, R=0.69, P<0.01) among the 20 genotypes; total As concentration (R=-0.67, P<0.01) and inorganic As concentration (R=-0.47, P<0.05) in rice grains of different genotypes were negatively correlated with ROL. There were also significant genotype effects in percentage inorganic As (F=15.8, P<0.001) and percentage cacodylic acid (F=22.1, P<0.001), respectively. Root aeration of different genotypes and variation of genotypes on As accumulation and speciation would be useful for selecting genotypes to grow in areas contaminated by As.     

Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution

Root system architecture depends on nutrient availability, which shapes primary and lateral root development in a nutrient-specific manner. To better understand how nutrient signals are integrated into root developmental programs, we investigated the morphological response of Arabidopsis thaliana roots to iron (Fe). Relative to a homogeneous supply, localized Fe supply in horizontally separated agar plates doubled lateral root length without having a differential effect on lateral root number. In the Fe uptake-defective mutant iron-regulated transporter1 (irt1), lateral root development was severely repressed, but a requirement for IRT1 could be circumvented by Fe application to shoots, indicating that symplastic Fe triggered the local elongation of lateral roots. The Fe-stimulated emergence of lateral root primordia and root cell elongation depended on the rootward auxin stream and was accompanied by a higher activity of the auxin reporter DR5-β-glucuronidase in lateral root apices. A crucial role of the auxin transporter AUXIN RESISTANT1 (AUX1) in Fe-triggered lateral root elongation was indicated by Fe-responsive AUX1 promoter activities in lateral root apices and by the failure of the aux1-T mutant to elongate lateral roots into Fe-enriched agar patches. We conclude that a local symplastic Fe gradient in lateral roots upregulates AUX1 to accumulate auxin in lateral root apices as a prerequisite for lateral root elongation.     

Root-induced changes in radial oxygen loss, rhizosphere oxygen profile, and nitrification of two rice cultivars in Chinese red soil regions

Aims

To evaluate the external and internal morphological differences of roots that might influence rice root radial oxygen loss (ROL) and the corresponding rhizosphere nitrification activity, growth characteristics and nitrogen nutrition of rice.

Methods

The root ROL and rhizosphere oxygen profile were determined using a miniaturised Clark-type oxygen microelectrode system, and the rhizosphere nitrification activity was studied with a short-term nitrification activity assay.

Results

The rice biomass, nitrogen accumulation and nitrogen use efficiency (NUE) of ZH (high yield) were significantly higher than those of HS (low yield). The root biomass, number, diameter and porosity of ZH were also much greater than those of HS. The inner and surface oxygen concentrations of the root of ZH were significantly higher than those of HS. The order of paddy soil oxygen penetration depth was ZH?>?HS?>?CK, and the order of the oxygen concentrations detected in the water layer and rhizosphere soil was the same. The rhizosphere nitrification activity and nitrate concentration of ZH were significantly higher than those of HS.

Conclusions

More porous and thicker roots improved the individual root ROL, and more adventitious root numbers enhanced the entire plant ROL and correspondingly improved the rhizosphere nitrification activity, which might influence the growth and nitrogen nutrition of rice.     

Negative phototropism of rice root and its influencing factors

Some characteristics of the rice (Oryza sativa L.) root were found in the experiment of unilaterally irradiating the roots which were planted in water: (i) All the seminal roots, adventitious roots and their branched roots bent away from light, and their curvatures ranged from 25℃ to 60℃. The curvature of adventitious root of the higher node was often larger than that of the lower node, and even larger than that of the seminal root. (ii) The negative phototropic bending of the rice root was mainly due to the larger growth increment of root-tip cells of the irradiated side compared with that of the shaded side, (iii) Root cap was the site of light perception. If root cap was shaded while the root was irradiated the root showed no negative phototropism, and the root lost the characteristic of negative phototropism when root cap was divested. Rice root could resume the characteristic of negative phototropism when the new root cap grew up, if the original cells of root cap were well protected while root ca     

Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths

Background and Aims

Many wetland species form aerenchyma and a barrier to radial O₂ loss (ROL) in roots. These features enhance internal O₂ 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.

Methods

ROL barrier induction in short and long roots of rice (Oryza sativa L. ‘Nipponbare’) was assessed using cylindrical root-sleeving O₂ electrodes and methylene blue indicator dye for O₂ leakage. Aerenchyma formation was also monitored in root cross-sections. Microstructure of hypodermal/exodermal layers was observed by transmission electron microscopy (TEM).

Key Results

In 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.

Conclusions

As 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.     

ANATOMY OF SEEDLING ROOTS OF PSEUDOTSUGA MENZIESII

The seedling root system of Pseudotsuga menziesii (Mirb.) Franco consists of the primary root, active long laterals, long laterals that become mycorrhizal, and short roots that may or may not become mycorrhizal. Numerous adventitious roots arise from the pericycle in young roots and from the vascular cambium and pericycle in older roots following pruning. All actively growing apices have a single plate of initials, a complex zonation of mother cells, and a similar pattern of primary tissue differentiation. Short roots and mycorrhizal short roots have 2 plates of initials, one producing the stele and the other the root cap and cortex, and differentiation occurs close to the apex. Primary and adventitious roots are usually triarch, while long laterals are usually diarch as are all short roots. The latter lack secondary xylem, but mycorrhizal short roots may produce a small amount of secondary phloem.     

Do radial oxygen loss and external aeration affect iron plaque formation and arsenic accumulation and speciation in rice?

Hydroponic experiments were conducted to investigate the effect of radial oxygen loss (ROL) and external aeration on iron (Fe) plaque formation, and arsenic (As) accumulation and speciation in rice (Oryza sativa L.). The data showed that there were significant correlations between ROL and Fe concentrations in Fe plaque produced on different genotypes of rice. There were also significant differences in the amounts of Fe plaque formed between different genotypes in different positions of roots and under different aeration conditions (aerated, normal, and stagnant treatments). In aerated treatments, rice tended to have a higher Fe plaque formation than in a stagnant solution, with the greatest formation at the root tip decreasing with increasing distances away, in accordance with a trend of spatial ROL. Genotypes with higher rates of ROL induced higher degrees of Fe plaque formation. Plaques sequestered As on rice roots, with arsenate almost double that with arsenite, leading to decreased As accumulation in both roots and shoots. The major As species detected in roots and shoots was arsenite, ranging from 34 to 78% of the total As in the different treatments and genotypes. These results contribute to our understanding of genotypic differences in As uptake by rice and the mechanisms causing rice genotypes with higher ROL to show lower overall As accumulation.     

Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology

We review the detrimental effects of waterlogging on physiology, growth and yield of wheat. We highlight traits contributing to waterlogging tolerance and genetic diversity in wheat. Death of seminal roots and restriction of adventitious root length due to O₂ deficiency result in low root:shoot ratio. Genotypes differ in seminal root anoxia tolerance, but mechanisms remain to be established; ethanol production rates do not explain anoxia tolerance. Root tip survival is short‐term, and thereafter, seminal root re‐growth upon re‐aeration is limited. Genotypes differ in adventitious root numbers and in aerenchyma formation within these roots, resulting in varying waterlogging tolerances. Root extension is restricted by capacity for internal O₂ movement to the apex. Sub‐optimal O₂ restricts root N uptake and translocation to the shoots, with N deficiency causing reduced shoot growth and grain yield. Although photosynthesis declines, sugars typically accumulate in shoots of waterlogged plants. Mn or Fe toxicity might occur in shoots of wheat on strongly acidic soils, but probably not more widely. Future breeding for waterlogging tolerance should focus on root internal aeration and better N‐use efficiency; exploiting the genetic diversity in wheat for these and other traits should enable improvement of waterlogging tolerance.     

Negative phototropism of rice root and its influencing factors

Some characteristics of the rice (Oryza sativa L.) root were found in the experiment of unilaterally irradiating the roots which were planted in water: (i) All the seminal roots, adventitious roots and their branched roots bent away from light, and their curvatures ranged from 25° to 60°. The curvature of adventitious root of the higher node was often larger than that of the lower node, and even larger than that of the seminal root, (ii) The negative phototropic bending of the rice root was mainly due to the larger growth increment of root-tip cells of the irradiated side compared with that of the shaded side, (iii) Root cap was the site of light perception. If root cap was shaded while the root was irradiated the root showed no negative phototropism, and the root lost the characteristic of negative phototropism when root cap was divested. Rice root could resume the characteristic of negative phototropism when the new root cap grew up, if the original cells of root cap were well protected while root cap was divested, (iv) The growth increment and curvature of rice root were both influenced by light intensity. Within the range of 0–100 μmol · m² -s⁻¹, the increasing of light intensity resulted in the decreasing of the growth increment and the increasing of the curvature of rice root, (v) The growth increment and the curvature reached the maximum at 30°C with the temperature treatment of 10–40°C. (vi) Blue-violet light could prominently induce the negative phototropism of rice root, while red light had no such effect. (vii) The auxin (IAA) in the solution, as a very prominent influencing factor, inhibited the growth, the negative phototropism and the gravitropism of rice root when the concentration of IAA increased. The response of negative phototropism of rice root disappeared when the concentration of IAA was above 10 mg · L⁻¹     

Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency

This study investigated aerenchyma formation and function in adventitious roots of wheat (Triticum aestivum L.) when only a part of the root system was exposed to O₂ deficiency. Two experimental systems were used: (1) plants in soil waterlogged at 200 mm below the surface; or (2) a nutrient solution system with only the apical region of a single root exposed to deoxygenated stagnant agar solution with the remainder of the root system in aerated nutrient solution. Porosity increased two‐ to three‐fold along the entire length of the adventitious roots that grew into the water‐saturated zone 200 mm below the soil surface, and also increased in roots that grew in the aerobic soil above the water‐saturated zone. Likewise, adventitious roots with only the tips growing into deoxygenated stagnant agar solution developed aerenchyma along the entire main axis. Measurements of radial O₂ loss (ROL), taken using root‐sleeving O₂ electrodes, showed this aerenchyma was functional in conducting O_2. The ROL measured near tips of intact roots in deoxygenated stagnant agar solution, while the basal part of the root remained in aerated solution, was sustained when the atmosphere around the shoot was replaced by N₂. This illustrates the importance of O₂ diffusion into the basal regions of roots within an aerobic zone, and the subsequent longitudinal movement of O₂ within the aerenchyma, to supply O₂ to the tip growing in an O₂ deficient zone.     

Ethylene induces epidermal cell death at the site of adventitious root emergence in rice

In deepwater rice (Oryza sativa), adventitious root primordia initiate at the nodes as part of normal development. Emergence of the roots is dependent on flooding of the plant and is mediated by ethylene action. Root growth was preceded by the induced death of epidermal cells of the node external to the tip of the root primordium. Cell death proceeded until the epidermis split open. Through this crack the root eventually emerged. Induced death was confined to nodal epidermal cells covering the tip of the primordia. Our results suggest that this process facilitates adventitious root emergence and prevents injury to the growing root. Cell death was inducible not only by submergence but also by application of 1-aminocyclopropane-1-carboxylic acid, the natural precursor of ethylene and it was suppressed in the presence of 2,5-norbornadiene (bicyclo[2.2.1]hepta-2,5-diene), an inhibitor of ethylene action. Adventitious root growth and epidermal cell death are therefore linked to the ethylene signaling pathway, which is activated in response to low oxygen stress.