Internal transport of gases is crucial for vascular plants inhabiting aquatic, wetland or flood-prone environments. Diffusivity of gases in water is approximately 10 000 times slower than in air; thus direct exchange of gases between submerged tissues and the environment is strongly impeded. Aerenchyma provides a low-resistance internal pathway for gas transport between shoot and root extremities. By this pathway, O2 is supplied to the roots and rhizosphere, while CO2, ethylene, and methane move from the soil to the shoots and atmosphere. Diffusion is the mechanism by which gases move within roots of all plant species, but significant pressurized through-flow occurs in stems and rhizomes of several emergent and floating-leaved wetland plants. Through-flows can raise O2 concentrations in the rhizomes close to ambient levels. In general, rates of flow are determined by plant characteristics such as capacity to generate positive pressures in shoot tissues, and resistance to flow in the aerenchyma, as well as environmental conditions affecting leaf-to-air gradients in humidity and temperature. O2 diffusion in roots is influenced by anatomical, morphological and physiological characteristics, and environmental conditions. Roots of many (but not all) wetland species contain large volumes of aerenchyma (e.g. root porosity can reach 55%), while a barrier impermeable to radial O2 loss (ROL) often occurs in basal zones. These traits act synergistically to enhance the amount of O2 diffusing to the root apex and enable the development of an aerobic rhizosphere around the root tip, which enhances root penetration into anaerobic substrates. The barrier to ROL in roots of some species is induced by growth in stagnant conditions, whereas it is constitutive in others. An inducible change in the resistance to O2 across the hypodermis/exodermis is hypothesized to be of adaptive significance to plants inhabiting transiently waterlogged soils. Knowledge on the anatomical basis of the barrier to ROL in various species is scant. Nevertheless, it has been suggested that the barrier may also impede influx of: (i) soil-derived gases, such as CO2, methane, and ethylene; (ii) potentially toxic substances (e.g. reduced metal ions) often present in waterlogged soils; and (iii) nutrients and water. Lateral roots, that remain permeable to O2, may be the main surface for exchange of substances between the roots and rhizosphere in wetland species. Further work is required to determine whether diversity in structure and function in roots of wetland species can be related to various niche habitats.

https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-3040.2003.00846.x

Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots

Geneticists and breeders are positioned to breed plants with root traits that improve productivity under drought. However, a better understanding of root functional traits and how traits are related to whole plant strategies to increase crop productivity under different drought conditions is needed. Root traits associated with maintaining plant productivity under drought include small fine root diameters, long specific root length, and considerable root length density, especially at depths in soil with available water. In environments with late season water deficits, small xylem diameters in targeted seminal roots save soil water deep in the soil profile for use during crop maturation and result in improved yields. Capacity for deep root growth and large xylem diameters in deep roots may also improve root acquisition of water when ample water at depth is available. Xylem pit anatomy that makes xylem less "leaky" and prone to cavitation warrants further exploration holding promise that such traits may improve plant productivity in water-limited environments without negatively impacting yield under adequate water conditions. Rapid resumption of root growth following soil rewetting may improve plant productivity under episodic drought. Genetic control of many of these traits through breeding appears feasible. Several recent reviews have covered methods for screening root traits but an appreciation for the complexity of root systems (e.g., functional differences between fine and coarse roots) needs to be paired with these methods to successfully identify relevant traits for crop improvement. Screening of root traits at early stages in plant development can proxy traits at mature stages but verification is needed on a case by case basis that traits are linked to increased crop productivity under drought. Examples in lesquerella (Physaria) and rice (Oryza) show approaches to phenotyping of root traits and current understanding of root trait genetics for breeding.

/pdf/root-traits-contributing-to-plant-productivity-under-drought-3jg834tnub.pdf

Root traits contributing to plant productivity under drought.

This article reviews the responses of plant roots to elevated rhizosphere cadmium (Cd) concentrations. Cadmium enters plants from the soil solution. It traverses the root through symplasmic or apoplasmic pathways before entering the xylem and being translocated to the shoot. Leaf Cd concentrations in excess of 5-10 μg g(-1) dry matter are toxic to most plants, and plants have evolved mechanisms to limit Cd translocation to the shoot. Cadmium movement through the root symplasm is thought to be restricted by the production of phytochelatins and the sequestration of Cd-chelates in vacuoles. Apoplasmic movement of Cd to the xylem can be restricted by the development of the exodermis, endodermis, and other extracellular barriers. Increasing rhizosphere Cd concentrations increase Cd accumulation in the plant, especially in the root. The presence of Cd in the rhizosphere inhibits root elongation and influences root anatomy. Cadmium concentrations are greater in the root apoplasm than in the root symplasm, and tissue Cd concentrations decrease from peripheral to inner root tissues. This article reviews current knowledge of the proteins involved in the transport of Cd across root cell membranes and its detoxification through sequestration in root vacuoles. It describes the development of apoplastic barriers to Cd movement to the xylem and highlights recent experiments indicating that their maturation is accelerated by high Cd concentrations in their immediate locality. It concludes that accelerated maturation of the endodermis in response to local Cd availability is of functional significance in protecting the shoot from excessive Cd loads.

Root responses to cadmium in the rhizosphere: a review

Without roots there would be no rhizosphere and no rhizodeposition to fuel microbial activity. Although micro-organisms may view roots merely as a source of carbon supply this belies the fascinating complexity and diversity of root systems that occurs despite their common function. Here, we examine the physiological and genetic determinants of root growth and the complex, yet varied and flexible, root architecture that results. The main functions of root systems are also explored including how roots cope with nutrient acquisition from the heterogeneous soil environment and their ability to form mutualistic associations with key soil micro-organisms (such as nitrogen fixing bacteria and mycorrhizal fungi) to aid them in their quest for nutrients. Finally, some key biotic and abiotic constraints on root development and function in the soil environment are examined and some of the adaptations roots have evolved to counter such stresses discussed.

Plant root growth, architecture and function

http://digital.csic.es/bitstream/10261/60376/4/Mesophyll_diffusion_conductance.pdf

Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis

A pressure chamber and a root pressure probe technique have been used to measure hydraulic conductivities of rice roots (root Lpr per m 2 of root surface area). Young plants of two rice (Oryza sativa L.) varieties (an upland variety, cv. Azucena and a lowland variety, cv. IR64) were grown for 31–40 d in 12 h days with 500 mmol m � 2 s � 1 PAR and dayunight temperatures of 27 8C and 22 8C. Root Lpr was measured under conditions of steady-state and transient water flow. Different growth conditions (hydroponic and aeroponic culture) did not cause visible differences in root anatomy in either variety. Values of root Lpr obtained from hydraulic (hydrostatic) and osmotic water flow were of the order of 10 � 8 ms � 1 MPa � 1 and were similar when using the different techniques. In comparison with other herbaceous species, rice roots tended to have a higher hydraulic resistance of the roots per unit root surface area. The data suggest that the low overall hydraulic conductivity of rice roots is caused by the existence of apoplastic barriers in the outer root parts (exodermis and sclerenchymatous (fibre) tissue) and by a strongly developed endodermis rather than by the existence of aerenchyma. According to the composite transport model of the root, the ability to adapt to higher transpirational demands from the shoot should be limited for rice because there were minimal changes in root Lpr depending on whether hydrostatic or osmotic forces were acting. It is concluded that this may be one of the reasons why rice suffers from water shortage in the shoot even in flooded fields.

Hydraulic conductivity of rice roots

The relative contribution of the apoplastic and cell-to-cell paths to the overall hydraulic conductivity of the outer part of rice roots (LpOPR) was estimated using a pressure perfusion technique for 30-d-old rice plants (lowland cultivar, IR64, and upland cultivar, Azucena). The technique was based on the perfusion of aerenchyma of root segments from two different zones (20-50 mm and 50-100 mm from the root apex) with aerated nutrient solution using precise pump rates. The outer part of roots (OPR) comprised an outermost rhizodermis, an exodermis, sclerenchyma fibre cells, and the innermost unmodified cortical cell layer. No root anatomical differences were observed for the two cultivars used. Development of apoplastic barriers such as Casparian bands and suberin lamellae in the exodermis were highly variable. On average, matured apoplastic barriers were observed at around 50-70 mm from the root apex. Lignification of the exodermis was completed earlier than that of sclerenchyma cells. Radial water flow across the OPR was impeded either by partially blocking off the porous apoplast with China ink particles (diameter 50 nm) or by closing water channels (aquaporins) in cell membranes with 50 micro M HgCl2. The reduction of LpOPR was relatively larger in the presence of an apoplastic blockage with ink ( approximately 30%) than in the presence of the water channel blocker ( approximately 10%) suggesting a relatively larger apoplastic water flow. The reflection coefficient of the OPR (sigmasOPR) for mannitol significantly increased during both treatments. It was larger when pores of the apoplast were closed, but absolute values were low (overall range of sigmasOPR=0.1-0.4), which also suggested a large contribution of the non-selective, apoplastic path to overall water flow. The strongest evidence in favour of a predominantly apoplastic water transport came from the comparison between diffusional (PdOPR, measured with heavy water, HDO) and osmotic water permeability (PfOPR) or hydraulic conductivity (LpOPR). PfOPR was larger by a factor of 600-1400 compared with P(dOPR). The development of OPR along roots resulted in a decrease of PdOPR by a factor of three (segments taken at 20-50 and 50-100 mm from root apex, respectively). Heat-killing of living cells resulted in an increase of PdOPR for both immature (20-50 mm) and mature (50-100 mm) root segments by a factor of two. Even though both pathways (apoplast and cell-to-cell) contributed to the overall water flow, the findings indicate predominantly apoplastic water flow across the OPR, even in the presence of apoplastic barriers. Low diffusional water permeabilities may suggest a low rate of oxygen diffusion across the OPR from aerenchyma to the outer anaerobic soil medium (low PO2OPR). To date, there are no data on PO2OPR. Provisional data of radial oxygen losses (ROL) across the OPR suggest that, unlike water, rice roots efficiently retain oxygen within the aerenchyma. This ability strongly increases as roots/OPR develop.

Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores

A new pressure-perfusion technique was used to measure hydraulic and osmotic properties of the outer part of roots (OPR) of 30-day-old rice plants (lowland cultivar: IR64, and upland cultivar: Azucena). The OPR comprised rhizodermis, exodermis, sclerenchyma and one cortical cell layer. The technique involved perfusion of aerenchyma of segments from two different root zones (20–50 mm and 50–100 mm from the tip) at precise rates using aerated nutrient solution. The hydraulic conductivity of the OPR (LpOPR=1.2×10−6 m s−1 MPa−1) was larger by a factor of 30 than the overall hydraulic conductivity (Lpr=4×10−8 m s−1 MPa−1) as measured by pressure chamber and root pressure probe. Low reflection coefficients were obtained for mannitol and NaCl for the OPR (σsOPR=0.14 and 0.09, respectively). The diffusional water permeability (P
 dOPR) estimated from isobaric flow of heavy water was smaller by three orders of magnitude than the hydraulic conductivity (LpOPR/P
 fOPR). Although detailed root anatomy showed well-defined Casparian bands and suberin lamellae in the exodermis, the findings strongly indicate a predominantly apoplastic water flow in the OPR. The LpOPR of heat-killed root segments increased by a factor of only 2, which is in line with the conclusion of a dominating apoplastic water flow. The hydraulic resistance of the OPR was not limiting the passage of water across the root cylinder. Estimations of the hydraulic properties of aerenchyma suggested that the endodermis was rate-limiting the water flow, although the aerenchyma may contribute to the overall resistance. The resistance of the aerenchyma was relatively low, because mono-layered cortical septa crossing the aerenchyma ('spokes') short-circuited the air space between the stele and the OPR. Spokes form hydraulic bridges that act like wicks. Low diffusional water permeabilities of the OPR suggest that radial oxygen losses from aerenchyma to medium are also low. It is concluded that in rice roots, water uptake and oxygen retention are optimized in such a way that hydraulic water flow can be kept high in the presence of a low efflux of oxygen which is diffusional in nature.

Control of water uptake by rice ( Oryza sativa L.): role of the outer part of the root

Precipitates of insoluble inorganic salts were used to clog apoplastic pores in cell walls of the outer part of rice roots (OPR) in two rice cultivars (lowland cv. IR64 and upland cv. Azucena). Aerenchyma of two different root zones (20‐ 50 and 50‐100 mm from the apex) was perfused with 1 m M potassium ferrocyanide (K 4 [Fe(CN) 6 ]) while the whole root segments were bathed in 0.5 m M copper sulphate (CuSO 4 ) medium. In another experiment, salts were applied on opposite sides of the OPR. The copper-ferrocyanide precipitation technique resembles the famous osmotic experiments of the German botanist Wilhelm Pfeffer, in which he used them with clay diaphragms. Precipitates were observed on the side where ferrocyanide was applied, suggesting that Cu 2 + and SO 4 2‐ were passing the barrier including the Casparian bands of the exodermis much faster than ferrocyanide. There was a patchiness in the formation of precipitates, correlated with the maturation of the exodermis. The intensity of copper ferrocyanide staining decreased along developing rice roots. No precipitates were observed in mature parts beyond 70‐80 mm from the root apex, except for sites around the emergence of secondary roots, which were fairly leaky to both water and ions. Blockage of the apoplastic pores with precipitates caused a three- to four-fold reduction of hydraulic conductivity of the OPR ( Lp OPR ). The reflection coefficient of the OPR ( s sOPR ) increased in response to the blockage with precipitates. The osmotic versus diffusive water permeability ratios of the OPR ( P fOPR / P dOPR ) were around 600 for immature and 1200 for mature root segments. Treatment significantly affected the bulk rather than the diffusive water flow and caused a three- to five-fold reduction of the P fOPR / P dOPR ratios. Results indicated that despite the existence of an exodermis with Casparian bands, most of the water moved around cells rather than using the cell-to-cell passage.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-3040.2004.01245.x

Renee Lafitte

Papers

Hydraulic conductivity of rice roots

Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores

Control of water uptake by rice ( Oryza sativa L.): role of the outer part of the root

Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell

QTLs affecting morph-physiological traits related to drought tolerance detected in overlapping introgression lines of rice (Oryza sativa L.)