Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize

Root phenes and phene states that reduce the metabolic cost of soil exploration may improve plant growth under low phosphorus availability. We tested the hypothesis that under low phosphorus, reduced living cortical area (LCA) would increase soil exploration, phosphorus capture, biomass, and grain yield. Maize genotypes contrasting in LCA were grown in the field and in greenhouse mesocosms under optimal and suboptimal phosphorus regimes. Percent LCA in nodal roots ranged from 25% to 67%. Plants with 0.2 mm² less LCA under low phosphorus had 75% less root segment respiration, 54% less root phosphorus content, rooted 20 cm deeper, allocated up to four times more roots between 60 and 120 cm depth, had between 20% and 150% more biomass, 35–40% greater leaf phosphorus content, and 60% greater grain yield compared with plants with high LCA. Low‐LCA plants had up to 55% less arbuscular mycorrhizal colonization in axial roots, but this decrease was not correlated with biomass or phosphorus content. The LCA components cortical cell file number and cortical cell size were important for biomass and phosphorus content under low phosphorus. These results are consistent with the hypothesis that root phenes that decrease the metabolic cost of soil exploration are adaptive under phosphorus stress.     

Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays)

Background and Aims

Formation of root cortical aerenchyma (RCA) can be induced by nutrient deficiency. In species adapted to aerobic soil conditions, this response is adaptive by reducing root maintenance requirements, thereby permitting greater soil exploration. One trade-off of RCA formation may be reduced radial transport of nutrients due to reduction in living cortical tissue. To test this hypothesis, radial nutrient transport in intact roots of maize (Zea mays) was investigated in two radiolabelling experiments employing genotypes with contrasting RCA.

Methods

In the first experiment, time-course dynamics of phosphate loading into the xylem were measured from excised nodal roots that varied in RCA formation. In the second experiment, uptake of phosphate, calcium and sulphate was measured in seminal roots of intact young plants in which variation in RCA was induced by treatments altering ethylene action or genetic differences.

Key Results

In each of three paired genotype comparisons, the rate of phosphate exudation of high-RCA genotypes was significantly less than that of low-RCA genotypes. In the second experiment, radial nutrient transport of phosphate and calcium was negatively correlated with the extent of RCA for some genotypes.

Conclusions

The results support the hypothesis that RCA can reduce radial transport of some nutrients in some genotypes, which could be an important trade-off of this trait.     

Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris)

Background and Aims

Root architectural phenes enhancing topsoil foraging are important for phosphorus acquisition. In this study, the utility of a novel phene is described, basal root whorl number (BRWN), that has significant effects on topsoil foraging in common bean (Phaseolus vulgaris).

Methods

Whorls are defined as distinct tiers of basal roots that emerge in a tetrarch fashion along the base of the hypocotyl. Wild and domesticated bean taxa as well as two recombinant inbred line (RIL) populations were screened for BRWN and basal root number (BRN). A set of six RILs contrasting for BRWN was evaluated for performance under low phosphorus availability in the greenhouse and in the field. In the greenhouse, plants were grown in a sand–soil media with low or high phosphorus availability. In the field, plants were grown in an Oxisol in Mozambique under low and moderate phosphorus availability.

Key Results

Wild bean accessions tended to have a BRWN of one or two, whereas cultivated accessions had BRWN reaching four and sometimes five. BRWN and BRN did not vary with phosphorus availability, i.e. BRWN was not a plastic trait in these genotypes. Greater BRWN was beneficial for phosphorus acquisition in low phosphorus soil. Genotypes with three whorls had almost twice the shoot biomass, greater root length and greater leaf area than related genotypes with two whorls. In low phosphorus soil, shoot phosphorus content was strongly correlated with BRWN (R² = 0·64 in the greenhouse and R² = 0·88 in the field). Genotypes with three whorls had shallower root systems with a greater range of basal root growth angles (from 10 to 45 ° from horizontal) than genotypes with two whorls (angles ranged from 60 to 85 ° from horizontal).

Conclusions

The results indicate that BRWN is associated with increased phosphorus acquisition and that this trait may have value for selection of genotypes with better performance in low phosphorus soils.     

Root cortical burden influences drought tolerance in maize

Background and Aims

Root cortical aerenchyma (RCA) increases water and nutrient acquisition by reducing the metabolic costs of soil exploration. In this study the hypothesis was tested that living cortical area (LCA; transversal root cortical area minus aerenchyma area and intercellular air space) is a better predictor of root respiration, soil exploration and, therefore, drought tolerance than RCA formation or root diameter.

Methods

RCA, LCA, root respiration, root length and biomass loss in response to drought were evaluated in maize (Zea mays) recombinant inbred lines grown with adequate and suboptimal irrigation in soil mesocosms.

Key Results

Root respiration was highly correlated with LCA. LCA was a better predictor of root respiration than either RCA or root diameter. RCA reduced respiration of large-diameter roots. Since RCA and LCA varied in different parts of the root system, the effects of RCA and LCA on root length were complex. Greater crown-root LCA was associated with reduced crown-root length relative to total root length. Reduced LCA was associated with improved drought tolerance.

Conclusions

The results are consistent with the hypothesis that LCA is a driver of root metabolic costs and may therefore have adaptive significance for water acquisition in drying soil.     

Lateral root development in the maize (Zea mays) lateral rootless1 mutant

Background and Aims

The maize lrt1 (lateral rootless1) mutant is impaired in its development of lateral roots during early post-embryonic development. The aim of this study was to characterize, in detail, the influences that the mutation exerts on lateral root initiation and the subsequent developments, as well as to describe the behaviour of the entire plant under variable environmental conditions.

Methods

Mutant lrt1 plants were cultivated under different conditions of hydroponics, and in between sheets of moist paper. Cleared whole mounts and anatomical sections were used in combination with both selected staining procedures and histochemical tests to follow root development. Root surface permeability tests and the biochemical quantification of lignin were performed to complement the structural data.

Key Results

The data presented suggest a redefinition of lrt1 function in lateral roots as a promoter of later development; however, neither the complete absence of lateral roots nor the frequency of their initiation is linked to lrt1 function. The developmental effects of lrt1 are under strong environmental influences. Mutant primordia are affected in structure, growth and emergence; and the majority of primordia terminate their growth during this last step, or shortly thereafter. The lateral roots are impaired in the maintenance of the root apical meristem. The primary root shows disturbances in the organization of both epidermal and subepidermal layers. The lrt1-related cell-wall modifications include: lignification in peripheral layers, the deposition of polyphenolic substances and a higher activity of peroxidase.

Conclusions

The present study provides novel insights into the function of the lrt1 gene in root system development. The lrt1 gene participates in the spatial distribution of initiation, but not in its frequency. Later, the development of lateral roots is strongly affected. The effect of the lrt1 mutation is not as obvious in the primary root, with no influences observed on the root apical meristem structure and maintenance; however, development of the epidermis and cortex are impaired.     

Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures

Background and Aims

During their domestication, maize, bean and squash evolved in polycultures grown by small-scale farmers in the Americas. Polycultures often overyield on low-fertility soils, which are a primary production constraint in low-input agriculture. We hypothesized that root architectural differences among these crops causes niche complementarity and thereby greater nutrient acquisition than corresponding monocultures.

Methods

A functional–structural plant model, SimRoot, was used to simulate the first 40 d of growth of these crops in monoculture and polyculture and to determine the effects of root competition on nutrient uptake and biomass production of each plant on low-nitrogen, -phosphorus and -potassium soils.

Key Results

Squash, the earliest domesticated crop, was most sensitive to low soil fertility, while bean, the most recently domesticated crop, was least sensitive to low soil fertility. Nitrate uptake and biomass production were up to 7 % greater in the polycultures than in the monocultures, but only when root architecture was taken into account. Enhanced nitrogen capture in polycultures was independent of nitrogen fixation by bean. Root competition had negligible effects on phosphorus or potassium uptake or biomass production.

Conclusions

We conclude that spatial niche differentiation caused by differences in root architecture allows polycultures to overyield when plants are competing for mobile soil resources. However, direct competition for immobile resources might be negligible in agricultural systems. Interspecies root spacing may also be too large to allow maize to benefit from root exudates of bean or squash. Above-ground competition for light, however, may have strong feedbacks on root foraging for immobile nutrients, which may increase cereal growth more than it will decrease the growth of the other crops. We note that the order of domestication of crops correlates with increasing nutrient efficiency, rather than production potential.     

Continuous,high-resolution biospeckle imaging reveals a discrete zone of activity at the root apex that responds to contact with obstacles

Background and Aims

Shining a laser onto biological material produces light speckles termed biospeckles. Patterns of biospeckle activity reflect changes in cell biochemistry, developmental processes and responses to the environment. The aim of this work was to develop methods to investigate the biospeckle activity in roots and to characterize the distribution of its intensity and response to thigmostimuli.

Methods

Biospeckle activity in roots of Zea mays, and also Jatropha curcas and Citrus limonia, was imaged live and in situ using a portable laser and a digital microscope with a spatial resolution of 10 μm per pixel and the ability to capture images every 0·080 s. A procedure incorporating a Fujii algorithm, image restoration using median and Gaussian filters, image segmentation using maximum-entropy threshold methods and the extraction of features using a tracing algorithm followed by spline fitting were developed to obtain quantitative information from images of biospeckle activity. A wavelet transform algorithm was used for spectral decomposition of biospeckle activity and generalized additive models were used to attribute statistical significance to changes in patterns of biospeckle activity.

Key Results

The intensity of biospeckle activity was greatest close to the root apex. Higher frequencies (3–6 Hz) contributed most to the total intensity of biospeckle activity. When a root encountered an obstacle, the intensity of biospeckle activity decreased abruptly throughout the root system. The response became attenuated with repeated thigmostimuli.

Conclusions

The data suggest that at least one component of root biospeckle activity resulted from a biological process, which is located in the zone of cell division and responds to thigmostimuli. However, neither individual cell division events nor root elongation is likely to be responsible for the patterns of biospeckle activity.     

Root foraging elicits niche complementarity-dependent yield advantage in the ancient ‘three sisters’ (maize/bean/squash) polyculture

MethodsMonocultures and polycultures of maize, bean and squash were grown in two seasons in field plots differing in nitrogen (N) and phosphorus (P) availability. Root growth patterns of individual crops and entire polycultures were determined using a modified DNA-based technique to discriminate roots of different species.ConclusionsIt is concluded that species differences in root foraging strategies increase total soil exploration, with consequent positive effects on the growth and yield of these ancient polycultures.     

An integrated method for quantifying root architecture of field-grown maize

Background and Aims

A number of techniques have recently been developed for studying the root system architecture (RSA) of seedlings grown in various media. In contrast, methods for sampling and analysis of the RSA of field-grown plants, particularly for details of the lateral root components, are generally inadequate.

Methods

An integrated methodology was developed that includes a custom-made root-core sampling system for extracting intact root systems of individual maize plants, a combination of proprietary software and a novel program used for collecting individual RSA information, and software for visualizing the measured individual nodal root architecture.

Key Results

Example experiments show that large root cores can be sampled, and topological and geometrical structure of field-grown maize root systems can be quantified and reconstructed using this method. Second- and higher order laterals are found to contribute substantially to total root number and length. The length of laterals of distinct orders varies significantly. Abundant higher order laterals can arise from a single first-order lateral, and they concentrate in the proximal axile branching zone.

Conclusions

The new method allows more meaningful sampling than conventional methods because of its easily opened, wide corer and sampling machinery, and effective analysis of RSA using the software. This provides a novel technique for quantifying RSA of field-grown maize and also provides a unique evaluation of the contribution of lateral roots. The method also offers valuable potential for parameterization of root architectural models.     

Carbon cost of root systems: an architectural approach

Root architecture is an important component of nutrient uptake and may be sensitive to carbon allocational changes brought about by rising CO₂. We describe a deformable geometric model of root growth, SimRoot, for the dynamic morphological and physiological simulation of root architectures. Using SimRoot, and measurements of root biomass deposition, respiration and exudation, carbon/phosphorus budgets were developed for three contrasting root architectures. Carbon allocation patterns and phosphorus acquisition efficiencies were estimated for Phaseolus vulgaris seedlings with either a dichotomous, herringbone, or empirically determined bean root architecture. Carbon allocation to biomass, respiration, and exudation varied significantly among architectures. Root systems also varied in the relationship between C expenditure and P acquisition, providing evidence for the importance of architecture in nutrient acquisition efficiency.     

Combined inoculation with Glomus intraradices and Rhizobium tropici CIAT899 increases phosphorus use efficiency for symbiotic nitrogen fixation in common bean (Phaseolus vulgaris L.)

This study compared the response of common bean (Phaseolus vulgaris L.) to arbuscular mycorrhizal fungi (AMF) and rhizobia strain inoculation. Two common bean genotypes i.e. CocoT and Flamingo varying in their effectiveness for nitrogen fixation were inoculated with Glomus intraradices and Rhizobium tropici CIAT899, and grown for 50 days in soil–sand substrate in glasshouse conditions. Inoculation of common bean plants with the AM fungi resulted in a significant increase in nodulation compared to plants without inoculation. The combined inoculation of AM fungi and rhizobia significantly increased various plant growth parameters compared to simple inoculated plants. In addition, the combined inoculation of AM fungi and rhizobia resulted in significantly higher nitrogen and phosphorus accumulation in the shoots of common bean plants and improved phosphorus use efficiency compared with their controls, which were not dually inoculated. It is concluded that inoculation with rhizobia and arbuscular mycorrhizal fungi could improve the efficiency in phosphorus use for symbiotic nitrogen fixation especially under phosphorus deficiency.     

A new species of Longitarsus Latreille, 1829 (Coleoptera, Chrysomelidae, Galerucinae) pupating inside stem aerenchyma of the hydrophyte host from the Oriental Region

A new species of subaquatic Longitarsus pupating inside the stem aerenchyma of its hydrophyte host plant is described. Eggs are laid on tender leaves and buds and the larvae are open feeders. This is the first report of an Oriental flea beetle pupating inside the stem of its hydrophyte host. A key to the species of southern Indian Longitarsus is provided.     

Near-isogenic lines for measuring phenotypic effects of DIMBOA-Glc methyltransferase activity in maize

Three O-methyltransferases (BX10a, b, c) catalyze the conversion of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside (DIMBOA-Glc) to 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA-Glc) in maize (Zea mays). Variation in benzoxazinoid accumulation and resistance to Rhopalosiphum maidis (corn leaf aphid) was attributed to a natural CACTA family transposon insertion that inactivates Bx10c. Whereas maize inbred line B73 has this transposon insertion, line CML277 does not. To characterize the phenotypic effects of DIMBOA-Glc methyltransferase activity, we created near-isogenic lines derived from B73 and CML277 that do or do not contain the transposon insertion. Bx10c inactivation causes high DIMBOA-Glc, low HDMBOA-Glc, and decreased aphid reproduction relative to near-isogenic lines that have a functional Bx10c gene. These results confirm the importance of this locus in maize aphid resistance. The availability of Bx10c near-isogenic lines will facilitate further research on the function of different benzoxazinoids and DIMBOA-Glc methyltransferase activity in maize defense against herbivores and pathogens.     

QTL analysis of root traits as related to phosphorus efficiency in soybean

Background and Aims

Low phosphorus (P) availability is a major constraint to soybean growth and production, especially in tropical and subtropical areas. Root traits have been shown to play critical roles in P efficiency in crops. Identification of the quantitative trait loci (QTLs) conferring superior root systems could significantly enhance genetic improvement in soybean P efficiency.

Methods

A population of 106 F₉ recombinant inbred lines (RILs) derived from a cross between BD2 and BX10, which contrast in both P efficiency and root architecture, was used for mapping and QTL analysis. Twelve traits were examined in acid soils. A linkage map was constructed using 296 simple sequence repeat (SSR) markers with the Kosambi function, and the QTLs associated with these traits were detected by composite interval mapping and multiple-QTL mapping.

Key Results

The first soybean genetic map based on field data from parental genotypes contrasting both in P efficiency and root architecture was constructed. Thirty-one putative QTLs were detected on five linkage groups, with corresponding contribution ratios of 9·1–31·1 %. Thirteen putative QTLs were found for root traits, five for P content, five for biomass and five for yield traits. Three clusters of QTLs associated with the traits for root and P efficiency at low P were located on the B1 linkage group close to SSR markers Satt519 and Satt519-Sat_128, and on the D2 group close to Satt458; and one cluster was on the B1 linkage group close to Satt519 at high P.

Conclusions

Most root traits in soybean were conditioned by more than two minor QTLs. The region closer to Satt519 on the B1 linkage group might have great potential for future genetic improvement for soybean P efficiency through root selection.     

Demonstration of osmotically dependent promotion of aerenchyma formation at different levels in the primary roots of rice using a 'sandwich' method and X-ray computed tomography

Background and Aims

The effect of environmental factors on the regulation of aerenchyma formation in rice roots has been discussed for a long time, because aerenchyma is constitutively formed under aerated conditions. To elucidate this problem, a unique method has been developed that enables sensitive detection of differences in the development of aerenchyma under two different environmental conditions. The method is tested to determine whether aerenchyma development in rice roots is affected by osmotic stress.

Methods

To examine aerenchyma formation both with and without mannitol treatment in the same root, germinating rice (Oryza sativa) caryopses were sandwiched between two agar slabs, one of which contained 270 mm of mannitol. The roots were grown touching both slabs and were thereby exposed unilaterally to osmotic stress. As a non-invasive approach, refraction contrast X-ray computed tomography (CT) using a third-generation synchrotron facility, SPring-8 (Super photon ring 8 GeV, Japan Synchrotron Radiation Research Institute), was used to visualize the three-dimensional (3-D) intact structure of aerenchyma and its formation in situ in rice roots. The effects of unilateral mannitol treatment on the development of aerenchyma were quantitatively examined using conventional light microscopy.

Key Results

Structural continuity of aerenchyma was clearly visualized in 3-D in the primary root of rice and in situ using X-ray CT. Light microscopy and X-ray CT showed that the development of aerenchyma was promoted on the mannitol-treated side of the root. Detailed light microscopic analysis of cross-sections cut along the root axis from the tip to the basal region demonstrated that aerenchyma developed significantly closer to the root tip on the mannitol-treated side of the root.

Conclusions

Continuity of the aerenchyma along the rice root axis was morphologically demonstrated using X-ray CT. By using this ‘sandwich’ method it was shown that mannitol promoted aerenchyma formation in the primary roots of rice.     

Modification of Resistance Expression of Phaseolus vulgaris to Meloidogyne incognita by Elevated Soil Temperatures

The effect of temperature on the reaction of susceptible (Canario Divex) and resistant (A 211) bean pure lines to Meloidogyne incognita was studied with soil temperature tanks housed in a growth chamber at 22 or 24 C. Soil temperature remained constant at 16, 22, 24, 26, 30, or 32 C in several trials. Bean line A 211 was resistant at 16 and 22 C but was susceptible at 24 C and above. Resistance to root-knot nematode reproduction was affected by a lower temperature (24 C) than was resistance to root galling (26 C) in A 211. Incubation of A 211 at 30 C for 3 and 16 days after inoculation with M. incognita resulted in a significant increase in nematode reproduction and root galling, respectively. The resistant reactions of A 211 to nematode reproduction and root galling were retained when inoculated plants were incubated at 21 C for a minimum of 16 and 23 days, respectively, prior to high temperature treatment.     

Influence of Maize Rotations on the Yield of Soybean Grown in Meloidogyne incognita Infested Soil

A replicated field study was conducted from 1972 to 1980 involving soybeans grown in 2-, 3-, and 4-year rotations with maize in soil infested with Meloidogyne incognita. Monocultured soybeans were maintained as controls. Cropping regimes involved root-knot nematode susceptible and resistant soybean cultivars and soybeans treated and not treated with nematicides. Yields of susceptible cultivars declined with reduced length of rotation. Nematicide treatment significantly increased yields of susceptible cultivars when monocultured, but bad little influence on yield when susceptible cultivars were grown in rotation. Yields of monocultured resistant cultivars were significantly lower than yields of resistant cultivars grown in rotation. However, yields of resistant cultivars grown in rotation were not influenced by the length of the rotation. Nematicide treatment significantly increased yields of monocultured resistant cultivars over the latter years of the study.     

Effects of Crop Rotation and Nonfumigant Nematicides on Peanut and Corn Yields in Fields Infested with Criconemella Species

The effects of nematicide treatments and corn-peanut cropping sequences on the population development of Criconemella ornata, and C. sphaerocephala and the related impact on crop yields were investigated at two North Carolina locations. Criconemella ornata and C. sphaerocephala were present at the Norman Perry farm, Bertie County (BERTIE); however, only C. ornata was found at the Central Crops Research Station, Johnston County (CCRS). An untreated control was compared to aldicarb 15G, carbofuran 15G, ethoprop 10G, and terbufos 15G granular formulations applied at a rate of 2.2 kg a.i./ha. The cropping sequences were monocuhured corn (C-C-C); monocultured peanut (P-P-P); and two corn-peanut (C-P-C; P-C-P) rotations. Nematicides were inconsistent in controlling C. sphaerocephala and C. ornata. Nematicide treatments enhanced corn yields in the monoculture-cropping cycle in the final year of the experiment at CCRS. Peanut yields were greater in the rotated cropping sequence than under monoculture at BERTIE, but rotation had less effect on peanut yields at CCRS. Declining yields were correlated with an increase in numbers of nematodes. Corn was an intermediate host for C. sphaerocephala and a moderate to poor host for C. ornata. Peanut was an excellent host for C. ornata and a poor host for C. sphaerocephala.