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1.  Characterization of a rice variety with high hydraulic conductance and identification of the chromosome region responsible using chromosome segment substitution lines 
Annals of Botany  2010;106(5):803-811.
Background and Aims
The rate of photosynthesis in paddy rice often decreases at noon on sunny days because of water stress, even under submerged conditions. Maintenance of higher rates of photosynthesis during the day might improve both yield and dry matter production in paddy rice. A high-yielding indica variety, ‘Habataki’, maintains a high rate of leaf photosynthesis during the daytime because of the higher hydraulic conductance from roots to leaves than in the standard japonica variety ‘Sasanishiki’. This research was conducted to characterize the trait responsible for the higher hydraulic conductance in ‘Habataki’ and identified a chromosome region for the high hydraulic conductance.
Hydraulic conductance to passive water transport and to osmotic water transport was determined for plants under intense transpiration and for plants without transpiration, respectively. The varietal difference in hydraulic conductance was examined with respect to root surface area and hydraulic conductivity (hydraulic conductance per root surface area, Lp). To identify the chromosome region responsible for higher hydraulic conductance, chromosome segment substitution lines (CSSLs) derived from a cross between ‘Sasanishiki’ and ‘Habataki’ were used.
Key Results
The significantly higher hydraulic conductance resulted from the larger root surface area not from Lp in ‘Habataki’. A chromosome region associated with the elevated hydraulic conductance was detected between RM3916 and RM2431 on the long arm of chromosome 4. The CSSL, in which this region was substituted with the ‘Habataki’ chromosome segment in the ‘Sasanishiki’ background, had a larger root mass than ‘Sasanishiki’.
The trait for increasing plant hydraulic conductance and, therefore, maintaining the higher rate of leaf photosynthesis under the conditions of intense transpiration in ‘Habataki’ was identified, and it was estimated that there is at least one chromosome region for the trait located on chromosome 4.
PMCID: PMC2958790  PMID: 20810742
Chromosome segment substitution lines; diffusive conductance; hydraulic conductance; photosynthetic rate; quantitative trait locus; rice; Oryza sativa; root hydraulic conductivity
2.  Role of adventitious roots in water relations of tamarack (Larix laricina) seedlings exposed to flooding 
BMC Plant Biology  2012;12:99.
Flooding reduces supply of oxygen to the roots affecting plant water uptake. Some flooding-tolerant tree species including tamarack (Larix laricina (Du Roi) K. Koch) produce adventitious roots in response to flooding. These roots were reported to have higher hydraulic conductivity under flooding conditions compared with non-adventitious roots. In the present study, we examined structural and functional modifications in adventitious roots of tamarack seedlings to explain their flooding tolerance.
Seedlings were subjected to the flooding treatment for six months, which resulted in an almost complete disintegration of the existing root system and its replacement with adventitious roots. We compared gas exchange parameters and water relations of flooded plants with the plants growing in well-drained soil and examined the root structures and root water transport properties. Although flooded seedlings had lower needle chlorophyll concentrations, their stomatal conductance, net photosynthesis rates and shoot water potentials were similar to non-flooded plants, indicative of flooding tolerance. Flooded adventitious roots had higher activation energy and a higher ratio of apoplastic to cell-to-cell water flow compared with non-flooded control roots as determined with the 1-hydroxypirene 3,6,8-trisulfonic acid apoplastic tracer dye. The adventitious roots in flooded plants also exhibited retarded xylem and endodermal development and accumulated numerous starch grains in the cortex. Microscopic examination of root sections treated with the PIP1 and PIP2 antibodies revealed high immunoreactivity in the cortex of non-flooded roots, as compared with flooded roots.
Structural modifications of adventitious roots suggest increased contribution of apoplastic bypass to water flow. The reduced dependence of roots on the hypoxia-sensitive aquaporin-mediated water transport is likely among the main mechanisms allowing tamarack seedlings to maintain water balance and gas exchange under flooding conditions.
PMCID: PMC3431261  PMID: 22738296
3.  Measurement of Leaf Hydraulic Conductance and Stomatal Conductance and Their Responses to Irradiance and Dehydration Using the Evaporative Flux Method (EFM) 
Water is a key resource, and the plant water transport system sets limits on maximum growth and drought tolerance. When plants open their stomata to achieve a high stomatal conductance (gs) to capture CO2 for photosynthesis, water is lost by transpiration1,2. Water evaporating from the airspaces is replaced from cell walls, in turn drawing water from the xylem of leaf veins, in turn drawing from xylem in the stems and roots. As water is pulled through the system, it experiences hydraulic resistance, creating tension throughout the system and a low leaf water potential (Ψleaf). The leaf itself is a critical bottleneck in the whole plant system, accounting for on average 30% of the plant hydraulic resistance3. Leaf hydraulic conductance (Kleaf = 1/ leaf hydraulic resistance) is the ratio of the water flow rate to the water potential gradient across the leaf, and summarizes the behavior of a complex system: water moves through the petiole and through several orders of veins, exits into the bundle sheath and passes through or around mesophyll cells before evaporating into the airspace and being transpired from the stomata. Kleaf is of strong interest as an important physiological trait to compare species, quantifying the effectiveness of the leaf structure and physiology for water transport, and a key variable to investigate for its relationship to variation in structure (e.g., in leaf venation architecture) and its impacts on photosynthetic gas exchange. Further, Kleaf responds strongly to the internal and external leaf environment3. Kleaf can increase dramatically with irradiance apparently due to changes in the expression and activation of aquaporins, the proteins involved in water transport through membranes4, and Kleaf declines strongly during drought, due to cavitation and/or collapse of xylem conduits, and/or loss of permeability in the extra-xylem tissues due to mesophyll and bundle sheath cell shrinkage or aquaporin deactivation5-10. Because Kleaf can constrain gs and photosynthetic rate across species in well watered conditions and during drought, and thus limit whole-plant performance they may possibly determine species distributions especially as droughts increase in frequency and severity11-14.
We present a simple method for simultaneous determination of Kleaf and gs on excised leaves. A transpiring leaf is connected by its petiole to tubing running to a water source on a balance. The loss of water from the balance is recorded to calculate the flow rate through the leaf. When steady state transpiration (E, mmol • m-2 • s-1) is reached, gs is determined by dividing by vapor pressure deficit, and Kleaf by dividing by the water potential driving force determined using a pressure chamber (Kleaf= E /- Δψleaf, MPa)15.
This method can be used to assess Kleaf responses to different irradiances and the vulnerability of Kleaf to dehydration14,16,17.
PMCID: PMC3577864  PMID: 23299126
Plant Biology; Issue 70; Molecular Biology; Physiology; Ecology; Biology; Botany; Leaf traits; hydraulics; stomata; transpiration; xylem; conductance; leaf hydraulic conductance; resistance; evaporative flux method; whole plant
4.  Root attributes affecting water uptake of rice (Oryza sativa) under drought 
Journal of Experimental Botany  2012;63(13):4751-4763.
Lowland rice roots have a unique physiological response to drought because of their adaptation to flooded soil. Rice root attributes that facilitate growth under flooded conditions may affect rice response to drought, but the relative roles of root structural and functional characteristics for water uptake under drought in rice are not known. Morphological, anatomical, biochemical, and molecular attributes of soil-grown rice roots were measured to investigate the genotypic variability and genotype×environment interactions of water uptake under variable soil water regimes. Drought-resistant genotypes had the lowest night-time bleeding rates of sap from the root system in the field. Diurnal fluctuation predominated as the strongest source of variation for bleeding rates in the field and root hydraulic conductivity (Lp r) in the greenhouse, and was related to expression trends of various PIP and TIP aquaporins. Root anatomy was generally more responsive to drought treatments in drought-resistant genotypes. Suberization and compaction of sclerenchyma layer cells decreased under drought, whereas suberization of the endodermis increased, suggesting differential roles of these two cell layers for the retention of oxygen under flooded conditions (sclerenchyma layer) and retention of water under drought (endodermis). The results of this study point to the genetic variability in responsiveness to drought of rice roots in terms of morphology, anatomy, and function.
PMCID: PMC3427995  PMID: 22791828
Aquaporin; drought; rice; root anatomy; root hydraulic conductivity; suberin
5.  Leaf Hydraulic Conductance for a Tank Bromeliad: Axial and Radial Pathways for Moving and Conserving Water 
Epiphytic plants in the Bromeliaceae known as tank bromeliads essentially lack stems and absorptive roots and instead take up water from reservoirs formed by their overlapping leaf bases. For such plants, leaf hydraulic conductance is plant hydraulic conductance. Their simple strap-shaped leaves and parallel venation make them suitable for modeling leaf hydraulic conductance based on vasculature and other anatomical and morphological traits. Plants of the tank bromeliad Guzmania lingulata were investigated in a lowland tropical forest in Costa Rica and a shaded glasshouse in Los Angeles, CA, USA. Stomatal conductance to water vapor and leaf anatomical variables related to hydraulic conductance were measured for both groups. Tracheid diameters and numbers of vascular bundles (veins) were used with the Hagen–Poiseuille equation to calculate axial hydraulic conductance. Measurements of leaf hydraulic conductance using the evaporative flux method were also made for glasshouse plants. Values for axial conductance and leaf hydraulic conductance were used in a model based on leaky cable theory to estimate the conductance of the radial pathway from the vein to the leaf surface and to assess the relative contributions of both axial and radial pathways. In keeping with low stomatal conductance, low stomatal density, low vein density, and narrow tracheid diameters, leaf hydraulic conductance for G. lingulata was quite low in comparison with most other angiosperms. Using the predicted axial conductance in the leaky cable model, the radial resistance across the leaf mesophyll was predicted to predominate; lower, more realistic values of axial conductance resulted in predicted radial resistances that were closer to axial resistance in their impact on total leaf resistance. Tracer dyes suggested that water uptake through the tank region of the leaf was not limiting. Both dye movement and the leaky cable model indicated that the leaf blade of G. lingulata was structurally and hydraulically well-suited to conserve water.
PMCID: PMC3622035  PMID: 23596446
epiphyte; leaky cable model; mesophyll conductance; monocot leaf; water relations; xylem
6.  Aerobic rice genotypes displayed greater adaptation to water-limited cultivation and tolerance to polyethyleneglycol-6000 induced stress 
Water scarcity and drought have seriously threatened traditional rice cultivation practices in several parts of the world including India. In the present investigation, experiments were conducted to see if the water-efficient aerobic rice genotypes developed at UAS, Bangalore (MAS25, MAS26 and MAS109) and IRRI, Philippines (MASARB25 and MASARB868), are endowed with drought tolerance or not. A set of these aerobic and five lowland high-yielding (HKR47 and PAU201, Taraori Basmati, Pusa1121 and Pusa1460) indica rice genotypes were evaluated for: (i) yield and yield components under submerged and aerobic conditions in field, (ii) root morphology and biomass under aerobic conditions in pots in the nethouse, (iii) PEG-6000 (0, −1, −2 and −3 bar) induced drought stress at vegetative stage using a hydroponic culture system and (iv) polymorphism for three SSR markers associated with drought resistance traits. Under submerged conditions, the yield of aerobic rice genotypes declined by 13.4–20.1 % whereas under aerobic conditions the yield of lowland indica/Basmati rice varieties declined by 23–27 %. Under water-limited conditions in pots, aerobic rice genotypes had 54–73.8 % greater root length and 18–60 % higher fresh root biomass compared to lowland indica rice varieties. Notably, root length of MASARB25 was 35 % shorter than MAS25 whereas fresh and dry root biomass of MASARB25 was 10 % and 64 % greater than MAS25. The lowland indica were more sensitive to PEG-stress with a score of 5.9–7.6 for Basmati and 6.1–6.7 for non-aromatic indica rice varieties, than the aerobic rice genotypes (score 2.7–3.3). A set of three microsatellite DNA markers (RM212, RM302 and RM3825) located on chromosome 1 which has been shown to be associated with drought resistance was investigated in the present study. Two of these markers (RM212 and RM302) amplified a specific allele in all the aerobic rice genotypes which were absent in lowland indica rice genotypes.
PMCID: PMC3550527  PMID: 23573038
Aerobic; Drought; Indica; Polyethyleneglycol 6000; Root traits; SSR
7.  The effects of water regime on phosphorus responses of rainfed lowland rice cultivars 
Annals of Botany  2008;103(2):211-220.
Background and Aims
Soil phosphorus (P) solubility declines sharply when a flooded soil drains, and an important component of rice (Oryza sativa) adaptation to rainfed lowland environments is the ability to absorb and utilize P under such conditions. The aim of this study was to test the hypothesis that rice cultivars differ in their P responses between water regimes because P uptake mechanisms differ.
Six lowland rice cultivars (three considered tolerant of low P soils, three sensitive) were grown in a factorial experiment with three water regimes (flooded, moist and flooded-then-moist) and four soil P levels, and growth and P uptake were measured. Small volumes of soil were used to maximize inter-root competition and uptake per unit root surface. The results were compared with the predictions of a model allowing for the effects of water regime on P solubility and diffusion.
Key Results
The plants were P stressed but not water stressed in all the water regimes at all P levels except the higher P additions in the flooded soil. The cultivar rankings scarcely differed between the water regimes and P additions. In all the treatments, the soil P concentrations required to explain the measured uptake were several times the concentration of freely available P in the soil.
The cultivar rankings were driven more by differences in growth habit than specific P uptake mechanisms, so the hypothesis cannot be corroborated with these data. Evidently all the plants could tap sparingly soluble forms of P by releasing a solubilizing agent or producing a greater root length than measured, or both. However, any cultivar differences in this were not apparent in greater net P uptake, possibly because the restricted rooting volume meant that additional P uptake could not be converted into new root growth to explore new soil volumes.
PMCID: PMC2707314  PMID: 18945744
Oryza sativa; rainfed lowland; phosphorus efficiency; root morphology; solubilization; rice cultivar
8.  Mild Salt Stress Conditions Induce Different Responses in Root Hydraulic Conductivity of Phaseolus vulgaris Over-Time 
PLoS ONE  2014;9(3):e90631.
Plants respond to salinity by altering their physiological parameters in order to maintain their water balance. The reduction in root hydraulic conductivity is one of the first responses of plants to the presence of salt in order to minimize water stress. Although its regulation has been commonly attributed to aquaporins activity, osmotic adjustment and the toxic effect of Na+ and Cl− have also a main role in the whole process. We studied the effects of 30 mM NaCl on Phaseolus vulgaris plants after 9 days and found different responses in root hydraulic conductivity over-time. An initial and final reduction of root hydraulic conductivity, stomatal conductance, and leaf water potential in response to NaCl was attributed to an initial osmotic shock after 1 day of treatment, and to the initial symptoms of salt accumulation within the plant tissues after 9 days of treatment. After 6 days of NaCl treatment, the increase in root hydraulic conductivity to the levels of control plants was accompanied by an increase in root fructose content, and with the intracellular localization of root plasma membrane aquaporins (PIP) to cortex cells close to the epidermis and to cells surrounding xylem vessels. Thus, the different responses of bean plants to mild salt stress over time may be connected with root fructose accumulation, and intracellular localization of PIP aquaporins.
PMCID: PMC3942473  PMID: 24595059
9.  Risk-taking plants 
Plant Signaling & Behavior  2012;7(7):767-770.
Water scarcity is a critical limitation for agricultural systems. Two different water management strategies have evolved in plants: an isohydric strategy and an anisohydric strategy. Isohydric plants maintain a constant midday leaf water potential (Ψleaf) when water is abundant, as well as under drought conditions, by reducing stomatal conductance as necessary to limit transpiration. Anisohydric plants have more variable Ψleaf and keep their stomata open and photosynthetic rates high for longer periods, even in the presence of decreasing leaf water potential. This risk-taking behavior of anisohydric plants might be beneficial when water is abundant, as well as under moderately stressful conditions. However, under conditions of intense drought, this behavior might endanger the plant. We will discuss the advantages and disadvantages of these two water-usage strategies and their effects on the plant’s ability to tolerate abiotic and biotic stress. The involvement of plant tonoplast AQPs in this process will also be discussed.
PMCID: PMC3583960  PMID: 22751307
abiotic stress; anisohydric; aquaporins; biotic stress; isohydric; leaf water potential; relative water content
10.  Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state 
Journal of Experimental Botany  2011;63(2):643-658.
Leaf hydraulic conductance (Kleaf) is a major determinant of photosynthetic rate in well-watered and drought-stressed plants. Previous work assessed the decline of Kleaf with decreasing leaf water potential (Ψleaf), most typically using rehydration kinetics methods, and found that species varied in the shape of their vulnerability curve, and that hydraulic vulnerability correlated with other leaf functional traits and with drought sensitivity. These findings were tested and extended, using a new steady-state evaporative flux method under high irradiance, and the function for the vulnerability curve of each species was determined individually using maximum likelihood for 10 species varying strongly in drought tolerance. Additionally, the ability of excised leaves to recover in Kleaf with rehydration was assessed, and a new theoretical framework was developed to estimate how rehydration of measured leaves may affect estimation of hydraulic parameters. As hypothesized, species differed in their vulnerability function. Drought-tolerant species showed shallow linear declines and more negative Ψleaf at 80% loss of Kleaf (P80), whereas drought-sensitive species showed steeper, non-linear declines, and less negative P80. Across species, the maximum Kleaf was independent of hydraulic vulnerability. Recovery of Kleaf after 1 h rehydration of leaves dehydrated below their turgor loss point occurred only for four of 10 species. Across species without recovery, a more negative P80 correlated with the ability to maintain Kleaf through both dehydration and rehydration. These findings indicate that resistance to Kleaf decline is important not only in maintaining open stomata during the onset of drought, but also in enabling sustained function during drought recovery.
PMCID: PMC3254676  PMID: 22016424
Cavitation; dehydration; EFM; Kleaf; rehydration; refilling; safety margins; turgor loss point; vulnerability curves
11.  Expression of ABA synthesis and metabolism genes under different irrigation strategies and atmospheric VPDs is associated with stomatal conductance in grapevine (Vitis vinifera L. cv Cabernet Sauvignon) 
Journal of Experimental Botany  2013;64(7):1907-1916.
The influence of different levels of irrigation and of variation in atmospheric vapour pressure deficit (VPD) on the synthesis, metabolism, and transport of abscisic acid (ABA) and the effects on stomatal conductance were examined in field-grown Cabernet Sauvignon grapevines. Xylem sap, leaf tissue, and root tissue were collected at regular intervals during two seasons in conjunction with measurements of leaf water potential (Ψleaf) and stomatal conductance (gs). The different irrigation levels significantly altered the Ψleaf and gs of the vines across both seasons. ABA abundance in the xylem sap was correlated with gs. The expression of genes associated with ABA synthesis, NCED1 and NCED2, was higher in the roots than in the leaves throughout and highest in the roots in mid January, a time when soil moisture declined and VPD was at its highest. Their expression in roots was also inversely related to the levels of irrigation and correlated with ABA abundance in the roots, xylem sap, and leaves. Three genes encoding ABA 8’-hydroxylases were isolated and their identities confirmed by expression in yeast cells. The expression of one of these, Hyd1, was elevated in leaves when VPD was below 2.0–2.5 kPa and minimal at higher VPD levels. The results provide evidence that ABA plays an important role in linking stomatal response to soil moisture status and that changes in ABA catabolism at or near its site of action allows optimization of gas exchange to current environmental conditions.
PMCID: PMC3638820  PMID: 23630325
Abscisic acid; ABA; ABA 8’-hydroxylase genes; grapevine; irrigation; NCED genes.
12.  Drought, Abscisic Acid and Transpiration Rate Effects on the Regulation of PIP Aquaporin Gene Expression and Abundance in Phaseolus vulgaris Plants 
Annals of Botany  2006;98(6):1301-1310.
• Background and Aims Drought causes a decline of root hydraulic conductance, which aside from embolisms, is governed ultimately by aquaporins. Multiple factors probably regulate aquaporin expression, abundance and activity in leaf and root tissues during drought; among these are the leaf transpiration rate, leaf water status, abscisic acid (ABA) and soil water content. Here a study is made of how these factors could influence the response of aquaporin to drought.
• Methods Three plasma membrane intrinsic proteins (PIPs) or aquaporins were cloned from Phaseolus vulgaris plants and their expression was analysed after 4 d of water deprivation and also 1 d after re-watering. The effects of ABA and of methotrexate (MTX), an inhibitor of stomatal opening, on gene expression and protein abundance were also analysed. Protein abundance was examined using antibodies against PIP1 and PIP2 aquaporins. At the same time, root hydraulic conductance (L), transpiration rate, leaf water status and ABA tissue concentration were measured.
• Key Results None of the treatments (drought, ABA or MTX) changed the leaf water status or tissue ABA concentration. The three treatments caused a decline in the transpiration rate and raised PVPIP2;1 gene expression and PIP1 protein abundance in the leaves. In the roots, only the drought treatment raised the expression of the three PIP genes examined, while at the same time diminishing PIP2 protein abundance and L. On the other hand, ABA raised both root PIP1 protein abundance and L.
• Conclusions The rise of PvPIP2;1 gene expression and PIP1 protein abundance in the leaves of P. vulgaris plants subjected to drought was correlated with a decline in the transpiration rate. At the same time, the increase in the expression of the three PIP genes examined caused by drought and the decline of PIP2 protein abundance in the root tissues were not correlated with any of the parameters measured.
PMCID: PMC2803586  PMID: 17028296
Abscisic acid; drought; methotrexate; Phaseolus vulgaris; plasma membrane aquaporins; root hydraulic conductance; transpiration rate
13.  Effect of Depth of Flooding on the Rice Water Weevil, Lissorhoptrus oryzophilus, and Yield of Rice 
The rice water weevil, Lissorhoptrus oryzophilus (Kuschel) (Coleoptera: Curculionidae), is a semi-aquatic pest of rice and is the most destructive insect pest of rice in the United States. Adults oviposit after floods are established, and greenhouse studies have shown that plants exposed to deep floods have more eggs oviposited in leaf sheaths than plants exposed to a shallow flood. Experiments were conducted in three mid-southern states in the USA to determine if the depth of flooding would impact numbers of L. oryzophilus on rice plants under field conditions. Rice was flooded at depths of approximately 5 or 10 cm in Arkansas in 2007 and 2008 and Louisiana in 2008, and at depths between 0–20 cm in Missouri in 2008. Plants were sampled three and four weeks after floods were established in all locations, and also two weeks after flood in Missouri. On all sampling dates in four experiments over two years and at three field sites, fewer L. oryzophilus larvae were collected from rice in shallow-flooded plots than from deep-flooded plots. The number of L. oryzophilus was reduced by as much as 27% in shallow-flooded plots. However, the reduction in insect numbers did not translate to a significant increase in rice yield. We discuss how shallow floods could be used as a component of an integrated pest management program for L. oryzophilus.
PMCID: PMC3740922  PMID: 23906324
cultural control; Oryza sativa; rice water weevil management
14.  Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors 
Journal of Experimental Botany  2009;61(3):821-829.
The slow-wilting soybean [Glycine max (L.) Merr.] genotype, PI 416937, exhibits a limiting leaf hydraulic conductance for transpiration rate (TR) under high vapour pressure deficit (VPD). This genotype has a constant TR at VPD greater than 2 kPa, which may be responsible for its drought tolerance as a result of soil water conservation. However, the exact source of the hydraulic limitation between symplastic and apoplastic water flow in the leaf under high VPD conditions are not known for PI 416937. A comparison was made in the TR response to aquaporin (AQP) inhibitors between PI 416937 and N01-11136, a commercial genotype that has a linear TR response to VPD in the 1–3.5 kPa range. Three AQP inhibitors were tested: cycloheximide (CHX, a de novo synthesis inhibitor), HgCl2, and AgNO3. Dose–response curves for the decrease in TR following exposure to each inhibitor were developed. Decreases in TR of N01-11136 following treatment with inhibitors were up to 60% for CHX, 82% for HgCl2, and 42% for AgNO3. These results indicate that the symplastic pathway terminating in the guard cells of these soybean leaves may be at least as important as the apoplastic pathway for water flow in the leaf under high VPD. While the decrease in TR for PI 416937 was similar to that of N01-11136 following exposure to CHX and HgCl2, TR of PI 416937 was insensitive to AgNO3 exposure. These results indicate the possibility of a lack of a Ag-sensitive leaf AQP population in the slow-wilting line, PI 416937, and the presence of such a population in the commercial line, N01-11136.
PMCID: PMC2814113  PMID: 19969533
Aquaporin; hydraulic flow; soybean; transpiration
15.  Water uptake by seminal and adventitious roots in relation to whole-plant water flow in barley (Hordeum vulgare L.) 
Journal of Experimental Botany  2010;62(2):717-733.
Prior to an assessment of the role of aquaporins in root water uptake, the main path of water movement in different types of root and driving forces during day and night need to be known. In the present study on hydroponically grown barley (Hordeum vulgare L.) the two main root types of 14- to 17-d-old plants were analysed for hydraulic conductivity in dependence of the main driving force (hydrostatic, osmotic). Seminal roots contributed 92% and adventitious roots 8% to plant water uptake. The lower contribution of adventitious compared with seminal roots was associated with a smaller surface area and number of roots per plant and a lower axial hydraulic conductance, and occurred despite a less-developed endodermis. The radial hydraulic conductivity of the two types of root was similar and depended little on the prevailing driving force, suggesting that water uptake occurred along a pathway that involved crossing of membrane(s). Exudation experiments showed that osmotic forces were sufficient to support night-time transpiration, yet transpiration experiments and cuticle permeance data questioned the significance of osmotic forces. During the day, 90% of water uptake was driven by a tension of about –0.15 MPa.
PMCID: PMC3003818  PMID: 20974734
Aquaporins; barley (Hordeum vulgare); cuticle; exudation; hydraulic conductivity; pressure probe; root water uptake; night-time transpiration
16.  Expression of Tolerance for Meloidogyne graminicola in Rice Cultivars as Affected by Soil Type and Flooding 
Journal of Nematology  2000;32(3):309-317.
The effects of different water regimes on the pathogenicity of Meloidogyne graminicola on six rice cultivars were determined in two soil types in three greenhouse experiments. Two water regimes, simulating continuous flooding and intermittent flooding, were used with five of the cultivars. All cultivars were susceptible to the nematode, but IR72 and IR74 were more tolerant than IR20 and IR29 under intermittent flooding. All were tolerant under continuous flooding. UPLRi-5 was grown under multiple water regimes: no flooding; continuous flooding; flooding starting at maximum tillering, panicle initiation, or booting stage; and flooding from sowing until maximum tillering or booting. In sandy loam soil, M. graminicola reduced stem and leaf dry weight, root dry weight, and grain weight under all water regimes. In clay loam soil, the nematode reduced root weight when the soil was not flooded or flooded only for a short time, from panicle initiation, or booting to maturity, and from sowing to maximum tillering. In clay loam soil, stem and leaf dry weight, as well as grain weight, were reduced by the nematode under all water regimes except continuous flooding or when the soil was flooded from sowing to booting stage. These results indicate that rice cultivar tolerance of M. graminicola varies with water regime and that yield losses due to M. graminicola may be prevented or minimized when the rice crop is flooded early and kept flooded until a late stage of development.
PMCID: PMC2620461  PMID: 19270982
Meloidogyne graminicola; pathogenicity; rice; tolerance; water regime
17.  Erythrina speciosa (Leguminosae-Papilionoideae) under soil water saturation: morphophysiological and growth responses 
Annals of Botany  2009;104(4):671-680.
Background and Aims
Erythrina speciosa is a Neotropical tree that grows mainly in moist habitats. To characterize the physiological, morphological and growth responses to soil water saturation, young plants of E. speciosa were subjected experimentally to soil flooding.
Flooding was imposed from 2 to 4 cm above the soil surface in water-filled tanks for 60 d. Non-flooded (control) plants were well watered, but never flooded. The net CO2 exchange (ACO2), stomatal conductance (gs) and intercellular CO2 concentration (Ci) were assessed for 60 d. Soluble sugar and free amino acid concentrations and the proportion of free amino acids were determined at 0, 7, 10, 21, 28 and 45 d of treatments. After 28, 45 and 60 d, dry masses of leaves, stems and roots were determined. Stem and root cross-sections were viewed using light microscopy.
Key Results
The ACO2 and gs were severely reduced by flooding treatment, but only for the first 10 d. The soluble sugars and free amino acids increased until the tenth day but decreased subsequently. The content of asparagine in the roots showed a drastic decrease while those of alanine and γ-aminobutyric increased sharply throughout the first 10 d after flooding. From the 20th day on, the flooded plants reached ACO2 and gs values similar to those observed for non-flooded plants. These events were coupled with the development of lenticels, adventitious roots and aerenchyma tissue of honeycomb type. Flooding reduced the growth rate and altered carbon allocation. The biomass allocated to the stem was higher and the root mass ratio was lower for flooded plants when compared with non-flooded plants.
Erythrina speciosa showed 100 % survival until the 60th day of flooding and was able to recover its metabolism. The recovery during soil flooding seems to be associated with morphological alterations, such as development of hypertrophic lenticels, adventitious roots and aerenchyma tissue, and with the maintenance of neutral amino acids in roots under long-term exposure to root-zone O2 deprivation.
PMCID: PMC2729630  PMID: 19581282
Erythrina speciosa; aerenchyma; amino acid content; biomass allocation; photosynthesis; flooding adaptations; stomatal conductance; O2 deficiency; γ-aminobutyric acid (GABA)
18.  Identification and characterization of genomic regions on chromosomes 4 and 8 that control the rate of photosynthesis in rice leaves 
Journal of Experimental Botany  2011;62(6):1927-1938.
DNA marker-assisted selection appears to be a promising strategy for improving rates of leaf photosynthesis in rice. The rate of leaf photosynthesis was significantly higher in a high-yielding indica variety, Habataki, than in the most popular Japanese variety, Koshihikari, at the full heading stage as a result of the higher level of leaf nitrogen at the same rate of application of nitrogen and the higher stomatal conductance even when the respective levels of leaf nitrogen were the same. The higher leaf nitrogen content of Habataki was caused by the greater accumulation of nitrogen by plants. The higher stomatal conductance of Habataki was caused by the higher hydraulic conductance. Using progeny populations and selected lines derived from a cross between Koshihikari and Habataki, it was possible to identify the genomic regions responsible for the rate of photosynthesis within a 2.1 Mb region between RM17459 and RM17552 and within a 1.2 Mb region between RM6999 and RM22529 on the long arm of chromosome 4 and on the short arm of chromosome 8, respectively. The designated region on chromosome 4 of Habataki was responsible for both the increase in the nitrogen content of leaves and hydraulic conductance in the plant by increasing the root surface area. The designated region on chromosome 8 of Habataki was responsible for the increase in hydraulic conductance by increasing the root hydraulic conductivity. The results suggest that it may be possible to improve photosynthesis in rice leaves by marker-assisted selection that focuses on these regions of chromosomes 4 and 8.
PMCID: PMC3060679  PMID: 21296764
Hydraulic conductance; hydraulic conductivity; leaf water potential; nitrogen content; photosynthetic rate; quantitative trait locus; rice; root surface area; stomatal conductance; water stress
19.  Seasonal changes of whole root system conductance by a drought-tolerant grape root system 
Journal of Experimental Botany  2010;62(1):99-109.
The role of root systems in drought tolerance is a subject of very limited information compared with above-ground responses. Adjustments to the ability of roots to supply water relative to shoot transpiration demand is proposed as a major means for woody perennial plants to tolerate drought, and is often expressed as changes in the ratios of leaf to root area (AL:AR). Seasonal root proliferation in a directed manner could increase the water supply function of roots independent of total root area (AR) and represents a mechanism whereby water supply to demand could be increased. To address this issue, seasonal root proliferation, stomatal conductance (gs) and whole root system hydraulic conductance (kr) were investigated for a drought-tolerant grape root system (Vitis berlandieri×V. rupestris cv. 1103P) and a non-drought-tolerant root system (Vitis riparia×V. rupestris cv. 101-14Mgt), upon which had been grafted the same drought-sensitive clone of Vitis vinifera cv. Merlot. Leaf water potentials (ψL) for Merlot grafted onto the 1103P root system (–0.91±0.02 MPa) were +0.15 MPa higher than Merlot on 101-14Mgt (–1.06±0.03 MPa) during spring, but dropped by approximately –0.4 MPa from spring to autumn, and were significantly lower by –0.15 MPa (–1.43±0.02 MPa) than for Merlot on 101-14Mgt (at –1.28±0.02 MPa). Surprisingly, gs of Merlot on the drought-tolerant root system (1103P) was less down-regulated and canopies maintained evaporative fluxes ranging from 35–20 mmol vine−1 s−1 during the diurnal peak from spring to autumn, respectively, three times greater than those measured for Merlot on the drought-sensitive rootstock 101-14Mgt. The drought-tolerant root system grew more roots at depth during the warm summer dry period, and the whole root system conductance (kr) increased from 0.004 to 0.009 kg MPa−1 s−1 during that same time period. The changes in kr could not be explained by xylem anatomy or conductivity changes of individual root segments. Thus, the manner in which drought tolerance was conveyed to the drought-sensitive clone appeared to arise from deep root proliferation during the hottest and driest part of the season, rather than through changes in xylem structure, xylem density or stomatal regulation. This information can be useful to growers on a site-specific basis in selecting rootstocks for grape clonal material (scions) grafted to them.
PMCID: PMC2993904  PMID: 20851906
Drought tolerance; grape; root hydraulic conductance; root hydraulic conductivity; root water relations; stomatal conductance; Vitis vinifera
20.  Molecular Breeding of Transgenic Rice Plants Expressing a Bacterial Chlorocatechol Dioxygenase Gene 
The cbnA gene encoding the chlorocatechol dioxygenase gene from Ralstonia eutropha NH9 was introduced into rice plants. The cbnA gene was expressed in transgenic rice plants under the control of a modified cauliflower mosaic virus 35S promoter. Western blot analysis using anti-CbnA protein indicated that the cbnA gene was expressed in leaf tissue, roots, culms, and seeds. Transgenic rice calluses expressing the cbnA gene converted 3-chlorocatechol to 2-chloromucote efficiently. Growth and morphology of the transgenic rice plants expressing the cbnA gene were not distinguished from those of control rice plants harboring only a Ti binary vector. It is thus possible to breed transgenic plants that degrade chloroaromatic compounds in soil and surface water.
PMCID: PMC123993  PMID: 12147507
21.  Hydraulic conductance as well as nitrogen accumulation plays a role in the higher rate of leaf photosynthesis of the most productive variety of rice in Japan 
Journal of Experimental Botany  2011;62(11):4067-4077.
An indica variety Takanari is known as one of the most productive rice varieties in Japan and consistently produces 20–30% heavier dry matter during ripening than Japanese commercial varieties in the field. The higher rate of photosynthesis of individual leaves during ripening has been recognized in Takanari. By using pot-grown plants under conditions of minimal mutual shading, it was confirmed that the higher rate of leaf photosynthesis is responsible for the higher dry matter production after heading in Takanari as compared with a japonica variety, Koshihikari. The rate of leaf photosynthesis and shoot dry weight became larger in Takanari after the panicle formation and heading stages, respectively, than in Koshihikari. Roots grew rapidly in the panicle formation stage until heading in Takanari compared with Koshihikari. The higher rate of leaf photosynthesis in Takanari resulted not only from the higher content of leaf nitrogen, which was caused by its elevated capacity for nitrogen accumulation, but also from higher stomatal conductance. When measured under light-saturated conditions, stomatal conductance was already decreased due to the reduction in leaf water potential in Koshihikari even under conditions of a relatively small difference in leaf–air vapour pressure difference. In contrast, the higher stomatal conductance was supported by the maintenance of higher leaf water potential through the higher hydraulic conductance in Takanari with the larger area of root surface. However, no increase in root hydraulic conductivity was expected in Takanari. The larger root surface area of Takanari might be a target trait in future rice breeding for increasing dry matter production.
PMCID: PMC3134360  PMID: 21527630
Dry matter production; high-yielding variety; hydraulic conductance; hydraulic conductivity; leaf nitrogen; photosynthesis; rice (Oryza sativa); ribulose-1; 5-bisphosphate carboxylase/oxygenase (Rubisco); root surface area; stomatal conductance
22.  A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea 
Journal of Experimental Botany  2011;62(12):4239-4252.
Chickpea is mostly grown on stored soil moisture, and deep/profuse rooting has been hypothesized for almost three decades to be critical for improving chickpea tolerance to terminal drought. However, temporal patterns of water use that leave water available for reproduction and grain filling could be equally critical. Therefore, variation in water use pattern and root depth/density were measured, and their relationships to yield tested under fully irrigated and terminal drought stress, using lysimeters that provided soil volumes equivalent to field conditions. Twenty chickpea genotypes having similar plant phenology but contrasting for a field-derived terminal drought-tolerance index based on yield were used. The pattern of water extraction clearly discriminated tolerant and sensitive genotypes. Tolerant genotypes had a lower water uptake and a lower index of stomatal conductance at the vegetative stage than sensitive ones, while tolerant genotypes extracted more water than sensitive genotypes after flowering. The magnitude of the variation in root growth components (depth, length density, RLD, dry weight, RDW) did not distinguish tolerant from sensitive genotypes. The seed yield was not significantly correlated with the root length density (RLD) in any soil layers, whereas seed yield was both negatively related to water uptake between 23–38 DAS, and positively related to water uptake between 48–61 DAS. Under these conditions of terminal drought, the most critical component of tolerance in chickpea was the conservative use of water early in the cropping cycle, explained partly by a lower canopy conductance, which resulted in more water available in the soil profile during reproduction leading to higher reproductive success.
PMCID: PMC3153682  PMID: 21610017
Chickpea; drought; lysimeter; roots; terminal drought; water use pattern; yield
23.  Water Use Efficiency and Physiological Response of Rice Cultivars under Alternate Wetting and Drying Conditions 
The Scientific World Journal  2012;2012:287907.
One of the technology options that can help farmers cope with water scarcity at the field level is alternate wetting and drying (AWD). Limited information is available on the varietal responses to nitrogen, AWD, and their interactions. Field experiments were conducted at the International Rice Research Institute (IRRI) farm in 2009 dry season (DS), 2009 wet season (WS), and 2010 DS to determine genotypic responses and water use efficiency of rice under two N rates and two water management treatments. Grain yield was not significantly different between AWD and continuous flooding (CF) across the three seasons. Interactive effects among variety, water management, and N rate were not significant. The high yield was attributed to the significantly higher grain weight, which in turn was due to slower grain filling and high leaf N at the later stage of grain filling of CF. AWD treatments accelerated the grain filling rate, shortened grain filling period, and enhanced whole plant senescence. Under normal dry-season conditions, such as 2010 DS, AWD reduced water input by 24.5% than CF; however, it decreased grain yield by 6.9% due to accelerated leaf senescence. The study indicates that proper water management greatly contributes to grain yield in the late stage of grain filling, and it is critical for safe AWD technology.
PMCID: PMC3539349  PMID: 23319883
24.  Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass 
Journal of Experimental Botany  2008;59(12):3317-3325.
Responses of plant leaf stomatal conductance and photosynthesis to water deficit have been extensively reported; however, little is known concerning the relationships of stomatal density with regard to water status and gas exchange. The responses of stomatal density to leaf water status were determined, and correlation with specific leaf area (SLA) in a photosynthetic study of a perennial grass, Leymus chinensis, subjected to different soil moisture contents. Moderate water deficits had positive effects on stomatal number, but more severe deficits led to a reduction, described in a quadratic parabolic curve. The stomatal size obviously decreased with water deficit, and stomatal density was positively correlated with stomatal conductance (gs), net CO2 assimilation rate (An), and water use efficiency (WUE). A significantly negative correlation of SLA with stomatal density was also observed, suggesting that the balance between leaf area and its matter may be associated with the guard cell number. The present results indicate that high flexibilities in stomatal density and guard cell size will change in response to water status, and this process may be closely associated with photosynthesis and water use efficiency.
PMCID: PMC2529243  PMID: 18648104
Gas exchange; guard cell size; photosynthesis; stomatal density; water stress; water use efficiency (WUE)
25.  Detecting the Differences in Responses of Stomatal Conductance to Moisture Stresses between Deciduous Shrubs and Artemisia Subshrubs 
PLoS ONE  2013;8(12):e84200.
Shrubs and subshrubs can tolerate wider ranges of moisture stresses in both soil and air than other plant life forms, and thus represent greater nonlinearity and uncertainty in ecosystem physiology. The objectives of this paper are to model shrub/subshrub stomatal conductance by synthesizing the field leaf gas exchanges data of 24 species in China, in order to detect the differences between deciduous shrubs and Artemisia subshrubs in their responses of stomatal conductance to changes in the moisture stresses. We revised a model of stomatal conductance by incorporating the tradeoff between xylem hydraulic efficiency and cavitation loss risk. We then fit the model at the three hierarchical levels: global (pooling all data as a single group), three functional groups (deciduous non-legume shrubs, deciduous legume shrubs, and subshrubs in Artemisia genus), and individual observations (species × sites). Bayesian inference with Markov Chain Monte Carlo method was applied to obtain the model parameters at the three levels. We found that the model at the level of functional groups is a significant improvement over that at the global level, indicating the significant differences in the stomatal behavior among the three functional groups. The differences in tolerance and sensitivities to changes in moisture stresses are the most evident between the shrubs and the subshrubs: The two shrub groups can tolerate much higher soil water stress than the subshrubs. The analysis at the observation level is also a significant improvement over that at the functional group level, indicating great variations within each group. Our analysis offered a clue for the equivocal issue of shrub encroachment into grasslands: While the invasion by the shrubs may be irreversible, the dominance of subshrubs, due to their lower resistance and tolerance to moisture stresses, may be put down by appropriate grassland management.
PMCID: PMC3875489  PMID: 24386351

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