Increased seminal root number associated with domestication improves nitrogen and phosphorus acquisition in maize seedlings

Background and AimsDomesticated maize (Zea mays ssp. mays) generally forms between two and six seminal roots, while its wild ancestor, Mexican annual teosinte (Zea mays ssp. parviglumis), typically lacks seminal roots. Maize also produces larger seeds than teosinte, and it generally has higher growth rates as a seedling. Maize was originally domesticated in the tropical soils of southern Mexico, but it was later brought to the Mexican highlands before spreading to other parts of the continent, where it experienced different soil resource constraints. The aims of this study were to understand the impacts of increased seminal root number on seedling nitrogen and phosphorus acquisition and to model how differences in maize and teosinte phenotypes might have contributed to increased seminal root number in domesticated maize.MethodsSeedling root system architectural models of a teosinte accession and a maize landrace were constructed by parameterizing the functional–structural plant model OpenSimRoot using plants grown in mesocosms. Seedling growth was simulated in a low-phosphorus environment, multiple low-nitrogen environments, and at variable planting densities. Models were also constructed to combine individual components of the maize and teosinte phenotypes.Key ResultsSeminal roots contributed ~35 % of the nitrogen and phosphorus acquired by maize landrace seedlings in the first 25 d after planting. Increased seminal root number improved plant nitrogen acquisition under low-nitrogen environments with varying precipitation patterns, fertilization rates, soil textures and planting densities. Models suggested that the optimal number of seminal roots for nutrient acquisition in teosinte is constrained by its limited seed carbohydrate reserves.ConclusionsSeminal roots can improve the acquisition of both nitrogen and phosphorus in maize seedlings, and the increase in seed size associated with maize domestication may have facilitated increased seminal root number.     

Morphological and architectural development of root systems in sorghum and maize

Root systems determine the capacity of a plant to access soil water and their architecture can influence adaptation to water-limited conditions. It may be possible to associate that architecture with root attributes of young plants as a basis for rapid phenotypic screening. This requires improved understanding of root system development. This study aimed to characterise the morphological and architectural development of sorghum and maize root systems by (i) clarifying the initiation and origin of roots at germination, and (ii) monitoring and quantifying the development of root systems in young plants. Three experiments were conducted with two maize and four sorghum hybrids. Sorghum produced a sole seminal (primary) root and coleoptile nodal roots emerged at the 4th–5th leaf stage, whereas maize produced 3–7 seminal (primary and scutellum) roots and coleoptile nodal roots emerged at the 2nd leaf stage. Genotypic variation in the flush angle and mean diameter of nodal roots was observed and could be considered a suitable target for large scale screening for root architecture in breeding populations. Because of the relatively late appearance of nodal roots in sorghum, such screening would require a small chamber system to grow plants until at least 6 leaves had fully expanded.     

Anatomy of Seedling Roots of Tropical Maize (Zea mays L.) Cultivars at Low Water Supply

Establishment of maize seedlings can be difficult at low soilmoisture content. Anatomy of root metaxylem vessels may influencethe capacity for water transport and respective genotypic differencesmight be useful for selection purposes. To test this, six tropicalmaize (Zea mays L.) cultivars were grown in large PVC tubescontaining a sandy substrate at 5% (M5) and 10% (M10) moisturecontents for 2 weeks. The percentage changes in root diametersdue to M5 was similar for most cultivars but differed for mainroot types. Root diameters were not consistently related tometaxylem structure, but in a few cases, thin roots had smallerdiameter metaxylem vessels. The M5 treatment reduced the numberof late metaxylem vessels of primary roots by about 0 to 20%,while effects on nodal roots were slight. Generally, the ratioof cross-sectional areas between late and early metaxylem vesselsincreased from primary to seminal and nodal roots. Within thecultivar Tuxpefio this ratio was much reduced by M5. A few cultivarsmaintained the combined cross-sectional areas of metaxylem vesselsat M5 in some main root types, but only one cultivar could achievethis for the total of cross-sectional areas of metaxylem vessels,calculated over all root axes, by increasing the number of seminaland nodal roots. These anatomical traits seemed to be mostlyconstitutive with limited response to an actual environment,but they could be decisive for the suitability of a cultivarto an environment with frequent water shortages during seedlingestablishment. Key words: Metaxylem vessels, water stress, tropical maize     

Plagiogravitropism of maize roots

The direction of root growth can be studied by analyzing the trajectories of roots growing in soil. Both the primary seminal root and nodal roots of maize attain a preferred, or liminal, angle of growth that deviates from the vertical. These roots are said to be plagiogravitropic. Experiments using plants grown in soil-filled boxes revealed that the primary seminal root is truly plagiogravitropic. It shows both positive and negative gravitropism in response to gravity stimuli and tends to maintain its direction even after growing around obstacles. These are experimental results suggesting that plagiogravitropic growth is controlled by internal factors. The orientation of the grain affects the establishment of the liminal angle of the primary seminal root, and both the position of their node of origin and the root diameter are closely related to the plagiogravitropic behaviour of nodal roots. Several external factors are also known to influence plagiogravitropism. Low soil water content causes a decrease in the angle of growth and soil mechanical resistance suppresses the gravitropic curvature. Plagiogravitropic behaviour of both seminal and nodal roots plays a significant role in shaping the root system.     

Biomechanics of nodal, seminal and lateral roots of barley: effects of diameter, waterlogging and mechanical impedance

Background and aims

Biomechanical properties of cereal root systems largely control both resistance to root lodging and their ability to stabilise soil. Abiotic stresses can greatly modify root system growth and form. In this paper the effect of waterlogging and moderate mechanical impedance on root biomechanics is studied for both lateral roots and the main axes of barley.

Methods

Barley (Hordeum vulgare) plants were subjected to transient water-logging and moderate mechanical impedance in repacked soil columns. Roots were excavated, separated into types (nodal, seminal or lateral) and tested in tension to measure strength and elastic modulus.

Results

Water-logging and mechanical impedance substantially changed root system growth whilst root biomechanical properties were affected by waterlogging. Root strength was generally greater in thin roots and depended on root type. For example, seminal roots 0.4–0.6 mm in diameter were approximately seven times stronger and five times stiffer than lateral roots of the same diameter when mechanically impeded. Root sample populations typically exhibited negative power-law relationships between root strength and diameter for all root types. Mechanical impedance slowed seminal root elongation by approximately 50 % and resulted in a 15 % and 11 % increase in the diameter of in nodal and seminal roots respectively. Power-law relationships between root diameter and root biomechanical properties corresponded to the different root types. Coefficients for between root diameter, strength and elastic modulus improved when separated by root type, with R² values increasing in some roots from 0.05 to 0.71 for root strength and 0.08 to 0.74 for elastic modulus.

Conclusions

Moderate mechanical impedance did not influence the tensile strength of roots, but, waterlogging diminished the relationship between root strength and diameter. Separation of root type improved predictions of root strength and elastic modulus using power-law regressions.     

Hemoglobin and Hypoxic Acclimation in Maize Root Tips

Class 1 hemoglobins (Hbs) have a wide distribution in the plant kingdom and have been demonstrated in root, seed, stem, and leaf tissues. They are present at low concentrations in aerobic tissue, but their synthesis is rapidly induced by hypoxic stress. The pattern of expression of the maize Hb gene in roots of young maize plants exposed to hypoxia has been examined. Root Hb gene expression increased rapidly to a maximum within first two hours of hypoxia, then declining to prehypoxia levels within 48-h hypoxic exposure. Limiting oxygen supply to the roots by total plant immersion and darkness did not alter the time course of hemoglobin expression. Hb gene expression was about 20-fold higher in the stele than in the cortex of control, aerobically grown roots. Stele Hb expression increased about fourfold under hypoxic conditions, whereas its expression in the cortex increased about 60-fold. In these samples, alcohol dehydrogenase (Adh) gene expression increased about four- and ten fold in the stele and cortex, respectively. The effect of the state of the Hb on anoxic survival of maize root tips was assessed by exposing root tips to a carbon monoxide atmosphere to maximize the proportion of hemoglobin in the carbonmonoxy form. Carbon monoxide had no significant effect on the survival or the ATP levels in anoxic maize roots, regardless of whether they had been acclimated by exposure to a hypoxic pretreatment. This would suggest that the presence of oxyhemoglobin is not essential for the survival of anoxic root tips.     

Enhancement of Anaerobic Respiration in Root Tips of Zea mays following Low-Oxygen (Hypoxic) Acclimation

Root tips (10-millimeter length) were excised from hypoxically pretreated (HPT, 4% [v/v] oxygen at 25°C for 16 hours) or nonhypoxically pretreated (NHPT, 40% [v/v] oxygen) maize (Zea mays) plants, and their rates of respiration were compared by respirometry under aerobic and anaerobic conditions with exogenous glucose. The respiratory quotient under aerobic conditions with 50 millimolar glucose was approximately 1.0, which is consistent with glucose or other hexose sugars being utilized as the predominant carbon source in glycolysis. Under strictly anaerobic conditions (anoxia), glycolysis was accelerated appreciably in both HPT and NHPT root tips, but the rate of anaerobic respiration quickly declined in NHPT roots. [U-¹⁴C]Glucose supplied under anaerobic conditions was taken up and respired by HPT root tips up to five times more rapidly than by NHPT roots. When anaerobic ethanol production was measured with excised root tips in 50 millimolar glucose, HPT tissues consistently produced ethanol more rapidly than NHPT tissues. These data suggest that a period of low oxygen partial pressure is necessary to permit adequate acclimation of the root tip of maize to subsequent anoxia, resulting in more rapid rates of fermentation and generation of ATP.     

MESOCOTYL ROOT FORMATION IN ECHINOCHLOA PHYLLOPOGON (POACEAE) IN RELATION TO ROOT ZONE AERATION

Echinochloa phyllopogon was grown hydroponically under four root zone gassing treatments to determine aeration effects on the growth and development of the plant root system. Although mesocotyl growth and the number of nodal roots were unaffected by the treatments, other aspects of plant growth were altered. Shoot growth was reduced by hypoxic (5 kPa partial pressure O₂ in nitrogen gas) and anoxic conditions (O₂ free nitrogen gas), but not by ethylene (0.1 ppm in air). Seminal root growth was unaffected by hypoxia or ethylene treatments, but was reduced under anoxia. Hypoxic environments stimulated the emergence of roots along the length of the mesocotyl when compared to aerobic controls; anoxic and ethylene treatments had no significant effects. Mesocotyl roots elongated from primordia that were produced de novo in response to the hypoxic treatment. Under hypoxic conditions, aerenchyma was present in the cortex of nodal roots and to a lesser extent in seminal roots, but mesocotyl roots were devoid of aerenchyma under these conditions. The results are compared with the literature concerning flooding and aeration effects on growth and development in other species.     

QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.)

Key message

QTL were identified for root architectural traits in maize.

Abstract

Root architectural traits, including the number, length, orientation, and branching of the principal root classes, influence plant function by determining the spatial and temporal domains of soil exploration. To characterize phenotypic patterns and their genetic control, three recombinant inbred populations of maize were grown for 28 days in solid media in a greenhouse and evaluated for 21 root architectural traits, including length, number, diameter, and branching of seminal, primary and nodal roots, dry weight of embryonic and nodal systems, and diameter of the nodal root system. Significant phenotypic variation was observed for all traits. Strong correlations were observed among traits in the same root class, particularly for the length of the main root axis and the length of lateral roots. In a principal component analysis, relationships among traits differed slightly for the three families, though vectors grouped together for traits within a given root class, indicating opportunities for more efficient phenotyping. Allometric analysis showed that trajectories of growth for specific traits differ in the three populations. In total, 15 quantitative trait loci (QTL) were identified. QTL are reported for length in multiple root classes, diameter and number of seminal roots, and dry weight of the embryonic and nodal root systems. Phenotypic variation explained by individual QTL ranged from 0.44 % (number of seminal roots, NyH population) to 13.5 % (shoot dry weight, OhW population). Identification of QTL for root architectural traits may be useful for developing genotypes that are better suited to specific soil environments.     

Metabolic response of river birch and European birch and European birch roots to hypoxia

Flood tolerance of woody plants has been attributed to internal oxygen diffusion from shoot to root, metabolic adaptation within the root, or both. The purpose of this study was to compare several biochemical and physiological responses of birch roots to hypoxia in order to determine the nature of root metabolic adaptation to low oxygen tension. One-year-old seedlings of flood-tolerant river birch (Betula nigra L.) and flood-intolerant European birch (Betula pendula Roth) were transferred to solution culture, and the solutions were bubbled with air or nitrogen. After 18 days of hypoxia, total adenosine phosphate and ATP contents of river birch roots were 35% and 23% of controls, respectively, whereas those of European birch roots were 13% and 8%. Adenylate energy charge of river birch roots decreased between 6 and 12 days of hypoxia. In contrast, energy charge of European birch roots decreased after only 1 day of hypoxia. In vitro activity of cytochrome c oxidase and oxygen consumption capacity of excised roots from both birch species decreased under hypoxia. In vitro activity of alcohol dehydrogenase from roots of both species increased after 1 day of hypoxia. However, alcohol dehydrogenase activity from river birch roots increased 25-fold after 6 days of hypoxia, whereas that from European birch decreased back to control levels. Hypoxia decreased malate content of roots from both species. Metabolic adaptation within the root, rather than internal oxygen diffusion, appears to be responsible for the relative tolerance of river birch to hypoxia.     

Cereal Cyst Nematode (Heterodera avenae) on Oats. II. Early Root Development and Nematode Tolerance

The effect of Heterodera avenae infestation on early seminal and lateral root growth was examined in four oat genotypes differing in tolerance to H. avenae. Recently emerged seminal roots were inoculated with a range of H. avenae larval densities, then transferred a hydroponic system to remove the effect of later nematode penetration on root development. Intolerance to H. avenae was assessed in terms of impairment of seminal root extension resulting in fewer primary lateral roots emerging from the seminal root below the zone of juvenile penetration. Tolerant plants infested with H. avenae had longer lateral root systems than infested intolerant plants. The decline in lateral root growth below the penetration zone was partly offset by increased growth above. This did not contribute to tolerance, however, as there were no differences between cultivars for this feature. Nematodes induced earlier nodal root emergence in all cultivars. Nodal root development was most advanced on the most tolerant cultivar.     

Steep,cheap and deep: an ideotype to optimize water and N acquisition by maize root systems

Background

A hypothetical ideotype is presented to optimize water and N acquisition by maize root systems. The overall premise is that soil resource acquisition is optimized by the coincidence of root foraging and resource availability in time and space. Since water and nitrate enter deeper soil strata over time and are initially depleted in surface soil strata, root systems with rapid exploitation of deep soil would optimize water and N capture in most maize production environments.• The ideotype Specific phenes that may contribute to rooting depth in maize include (a) a large diameter primary root with few but long laterals and tolerance of cold soil temperatures, (b) many seminal roots with shallow growth angles, small diameter, many laterals, and long root hairs, or as an alternative, an intermediate number of seminal roots with steep growth angles, large diameter, and few laterals coupled with abundant lateral branching of the initial crown roots, (c) an intermediate number of crown roots with steep growth angles, and few but long laterals, (d) one whorl of brace roots of high occupancy, having a growth angle that is slightly shallower than the growth angle for crown roots, with few but long laterals, (e) low cortical respiratory burden created by abundant cortical aerenchyma, large cortical cell size, an optimal number of cells per cortical file, and accelerated cortical senescence, (f) unresponsiveness of lateral branching to localized resource availability, and (g) low K_m and high V_max for nitrate uptake. Some elements of this ideotype have experimental support, others are hypothetical. Despite differences in N distribution between low-input and commercial maize production, this ideotype is applicable to low-input systems because of the importance of deep rooting for water acquisition. Many features of this ideotype are relevant to other cereal root systems and more generally to root systems of dicotyledonous crops.     

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.     

Changes in root system structure,leaf water potential and gas exchange of maize and triticale seedlings affected by soil compaction

The physiological reasons associated with differential sensitivity of C₃ and C₄ plant species to soil compaction stress are not well explained and understood. The responses of growth characteristics, changes in leaf water potential and gas exchange in maize and triticale to a different soil compaction were investigated. In the present study seedlings of triticale and maize, representative of C₃ and C₄ plants were subjected to low (L – 1.10 g cm⁻³), moderate (M – 1.34 g cm⁻³) and severe (S – 1.58 g cm⁻³) soil compaction level. Distinct differences in distribution of roots in the soil profile were observed. Plants of treatments M or S in comparison to treatment L, showed a decrease in leaf number, dry mass of stem, leaves and roots, and an increase in the shoot to root ratio. A drastic decrease in root biomass in M and S treatments in the soil profile on depth from 15 to 40 cm was observed. Any level of soil compaction did not influence the number of seminal and seminal-adventitious roots but decreased their length. The number and total length of nodal roots decreased with compaction. Changes of growth traits in M and S treatments in comparison to the L were greater for maize than for triticale and were accompanied by daily changes in water potential (ψ) and gas exchange parameters (P_N, E, g_s). Differences between M and S treatments in daily changes in ψ for maize were in most cases statistically insignificant, whereas for triticale, they were statistically significant. Differences in the responses of maize and triticale to soil compaction were found in P_N, E and g_s in particular for the measurements taken at 12:00 and 16:00. The highest correlation coefficients were obtained for the relationship between leaf water potential and stomatal conductance, both for maize and triticale, which indicates the close association between stomata behavior and changes in leaf water status.     

Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat

Abstract The present paper describes the effects of growth of roots of wheat (Triticum aestivum cv. Gamenya) in hypoxic nutrient solutions on acrenchyma formation and O₂ movement from shoots to roots. Two types of roots were investigated: (1) seminal roots of 4–7-d-old seedlings, and (2) seminal and nodal roots of 10–28-d-old plants. Gas-filled porosity of seminal and nodal roots increased from 3 to 12% and from 5–7 to 11–15%, respectively, when the roots emerged in stagnant or N₂-flushed solutions (0.003 mol m ^?3 O₂) compared with growth in continuously acrated solutions (0.26 mol m ^?3 O₂). However, neither root type increased in porosity when they were longer than 100–200 mm at the start of the exposure to these stagnant or N₂-flushed treatments. A vernier microscope and cylindrical platinum-electrode were used to examine the relationship between root extension and transport of O₂ from shoots to roots via the gas spaces. Measurements were made when the roots were in an anoxic medium and were dependent solely on O₂ supplied from the shoots. For seminal roots of 5–7-d-old seedlings raised in stagnant solutions (90–100 mm), internal O₂ transport was sufficient to support a rate of root elongation in the O₂-free medium of between 0.03 and 0.17 mm h^?1. When the O₂ pressure around the shoots was increased from 20 to 100 kPa O₂, the O₂ concentrations at the walls of the expanding zone (2–7 mm from the tip) of these roots increased from 0.006 mol m^?3 to between 0.04 and 0.26 mol m^?3, and the rate of root extension increased five-fold. Oxygen transport to roots grown continuously in acrated solutions was considerably less than for roots raised in stagnant solutions; this difference was greater for seminal than for nodal roots. When the acrated seminal roots were longer than 100 mm and transferred to an O₂-free root medium, O₂ concentration became zero at the root tip causing elongation to cease. After 24 h of anoxia, none of these roots were able to resume elongation following a return to acrated solutions.     

Ecophysiology of Wetland Plant Roots: A Modelling Comparison of Aeration in Relation to Species Distribution

This study examined the potential for inter-specific differencesin root aeration to determine wetland plant distribution innature. We compared aeration in species that differ in the typeof sediment and depth of water they colonize. Differences inroot anatomy, structure and physiology were applied to aerationmodels that predicted the maximum possible aerobic lengths anddevelopment of anoxic zones in primary adventitious roots. Differencesin anatomy and metabolism that provided higher axial fluxesof oxygen allowed deeper root growth in species that favourmore reducing sediments and deeper water. Modelling identifiedfactors that affected growth in anoxic soils through their effectson aeration. These included lateral root formation, which occurredat the expense of extension of the primary root because of theadditional respiratory demand they imposed, reducing oxygenfluxes to the tip and stele, and the development of stelar anoxia.However, changes in sediment oxygen demand had little detectableeffect on aeration in the primary roots due to their low wallpermeability and high surface impedance, but appeared to reduceinternal oxygen availability by accelerating loss from laterals.The development of pressurized convective gas flow in shootsand rhizomes was also found to be important in assisting rootaeration, as it maintained higher basal oxygen concentrationsat the rhizome–root junctions in species growing intodeep water. Copyright 2000 Annals of Botany Company Aeration, diffusion, ecophysiology, flooding, model, oxygen, respiration, root, wetland     

Interspecific differences in root architecture among maize and triticale genotypes grown under drought,waterlogging and soil compaction

Environmental stresses (soil compaction, drought, waterlogging) cause changes in plants’ root system structure, also affecting the growth of above-ground parts. The aim of this study was to estimate phenotypic variation among maize and triticale genotypes in root penetration ability through petrolatum-wax-layer (RPA). Also, the effect of shortage or excess of soil water on dry matter of shoots and roots and morphological changes in root system structure in sensitive and resistant maize and triticale genotypes grown in low or high soil compaction level was evaluated. To estimate RPA index, the petrolatum-wax-layer method (PWL) was used. The strength of three petrolatum-wax concentrations 60, 50 and 40 % was 0.52, 1.07 and 1.58 MPa, respectively. High coefficients of variation (CV) were observed in 0.52 and 1.07 MPa and for maize were 19.2 and 21.7 %, and for triticale, 12.5 and 18.3 %, respectively. The data indicate that the use of PWL technique is an effective screening method, and makes it possible to divide the genotypes into resistant and sensitive groups. The second part of this study investigated a multistress effect of soil compaction combined with drought or waterlogging on root and shoot growth and morphological changes in root system structure of maize and triticale genotypes differing in susceptibility to environmental stresses. Seedlings were grown for 4 weeks in root-boxes under conditions of low (LSC 1.1 g cm^?3) or severe (SSC 1.6 g cm^?3) soil compaction. Drought or waterlogging stresses were applied for 2 weeks from 14th to 28th day. In comparison to LSC treatment, in SSC treatment the decrease in dry matter of shoots and roots was greater for sensitive genotypes of maize and triticale (Ancora, CHD-147). Soil drought or waterlogging caused greater decrease of dry matter of shoots and roots in seedlings grown in SSC in comparison to LSC. The root penetration index (RPI) was estimated as a ratio of root dry matter in 15–40 cm root-box layer to total root dry matter. On the basis of RPI it was possible to group the genotypes according to their ability to distribute roots in soil profile. In comparison to LSC, SSC exerted a strong influence on the length of seminal and seminal adventitious roots, as well as the number and length of L- and S-type lateral roots developed on seminal and nodal roots. In both species the restriction effect of soil compaction on number and length of roots was more severe in sensitive (Ankora, CHD-147) than in resistant (Tina, CHD-247) genotypes. The restriction in roots propagation was greater in triticale than in maize. Exposure to drought or waterlogging in the case of genotypes grown in LSC and SSC treatments caused a decrease in number and length of particular components of root system structure. In both species the decrease of root number and length in plants grown under waterlogging was greater than under drought. The observed changes in root system were greater in sensitive (Ankora, CHD147) than in resistant (Tina, CHD-247) genotypes. Statistically significant correlations were found between RPA and RPI and also between these indexes and soil compaction, drought and waterlogging susceptibility indexes. This indicates that genotypes resistant to soil compaction were resistant to drought or waterlogging and also that genotypes resistant to drought were resistant to waterlogging.