QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean

The relationship between root-hair growth, acid exudation and phosphorus (P) uptake as well as the quantitative trait loci (QTLs) associated with these traits were determined for a recombinant inbred line (RIL) population derived from the cross of two contrasting common bean (Phaseolus vulgaris L.) genotypes, DOR364 and G19833, which were grown in solution culture and under field conditions with low-P availability. In the solution-culture study, root-hair density, root-hair length, H⁺ exudation and total acid exudation were measured. Substantial genotypic variability was observed for these traits and their response to P availability. The P-efficient parent G19833 had greater root-hair density, longer root-hair length, and greater exudation of H⁺ and total acid than the P-inefficient genotype DOR364. These traits segregated continuously in the RIL population, with obvious tendency of trait transgression. Genetic analysis revealed that the root traits measured had various heritabilities, with h _b ² ranging from 43.24 to 86.70%. Using an integrated genetic map developed for the population, a total of 19 QTLs associated with root hair, acid exudation and P-uptake traits were detected on 8 linkage groups. P uptake in the field was positively correlated with total acid exudation, basal root-hair length, and basal root-hair density. Acid-exudation traits were intercorrelated, as were root-hair traits. Total acid exudation was positively correlated with basal root-hair density and length. Linkage analysis revealed that some of the root-trait QTLs were closely linked with QTLs for P uptake in the field. We propose that marker-assisted selection (MAS) might be a feasible alternative to conventional screening of phenotypic root traits.     

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.     

Effects of phosphorus availability and vesicular–arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris)

Low phosphorus availability is often a primary constraint to plant productivity in native soils. Here we test the hypothesis that root carbon costs are a primary limitation to plant growth in low P soils by assessing the effect of P availability and mycorrhizal infection on whole plant C budgets in common bean ( Phaseolus vulgaris L.). Plants were grown in solid-phase-buffered silica sand providing a constant supply of low (1 μ m ) or moderate (10 μ m ) P. Carbon budgets were determined weekly during the vegetative growth phase. Mycorrhizal infection in low-P plants increased the root specific P absorption rate, but a concurrent increase in root respiration consumed the increased net C gain resulting from greater P uptake. The energy content of mycorrhizal and non-mycorrhizal roots was similar. We propose that the increase in root respiration in mycorrhizal roots was mainly due to increased maintenance and growth respiration of the fungal tissue. Plants grown with low P availability expended a significantly larger fraction of their total daily C budget on below-ground respiration at days 21, 28 and 35 after planting (29–40%) compared with plants grown with moderate P supply (18–25%). Relatively greater below-ground respiration in low P plants was mainly a result of their increased root:shoot ratio, although specific assimilation rate was reduced significantly at days 21 and 28 after planting. Specific root respiration was reduced over time by low P availability, by up to 40%. This reduction in specific root respiration was due to a reduction in ion uptake respiration and growth respiration, whereas maintenance respiration was increased in low-P plants. Our results support the hypothesis that root C costs are a primary limitation to plant growth in low-P soils.     

Ethylene: a regulator of root architectural responses to soil phosphorus availability

The involvement of ethylene in root architectural responses to phosphorus availability was investigated in common bean ( Phaseolus vulgaris L.) plants grown with sufficient and deficient phosphorus. Although phosphorus deficiency reduced root mass and lateral root number, main root length was unchanged by phosphorus treatment. This resulted in decreased lateral root density in phosphorus-deficient plants. The possible involvement of ethylene in growth responses to phosphorus deficiency was investigated by inhibiting endogenous ethylene production with amino-ethoxyvinylglycine (AVG) and aerating the root system with various concentrations of ethylene. Phosphorus deficiency doubled the root-to-shoot ratio, an effect which was suppressed by AVG and partially restored by exogenous ethylene. AVG increased lateral root density in phosphorus- deficient plants but reduced it in phosphorus-sufficient plants. These responses could be reversed by exogenous ethylene, suggesting ethylene involvement in the regulation of main root extension and lateral root spacing. Phosphorus-deficient roots produced twice as much ethylene per g dry matter as phosphorus-sufficient roots. Enhanced ethylene production and altered ethylene sensitivity in phosphorus-deficient plants may be responsible for root responses to phosphorus deficiency.     

Fractal geometry of root systems: Field observations of contrasting genotypes of common bean (Phaseolus vulgaris L.) grown under different phosphorus regimes

Root growth and architecture are important for phosphorus acquisition due to the relative immobility of P in the soil. Fractal geometry is a potential new approach to the analysis of root architecture. Substantial genetic variation in root growth and architecture has been observed in common bean. Common bean (Phaseolus vulgaris L.) genotypes with contrasting root architecture were grown under moderate and low P conditions in a field experiment. Linear and planar fractal dimension were measured by tracing root intercepts with vertical planes. Linear fractal dimension increased over time in efficient genotypes, but remained fairly constant over time in inefficient genotypes. Planar fractal dimension increased over time for all genotypes, but was higher in efficient than inefficient genotypes at the end of the experiment. Planar fractal dimension of medium P plants was found to correlate with shoot P content indicating fractal dimension to be a possible indicator for root P uptake. The increasing fractal dimension over time indicates that fractal analysis is a sensitive measure of root branching intensity. A less destructive method for acquisition of data that allows for continuous analysis of fractal geometry and thereby screening for more P efficient genotypes in the field is suggested. This method will allow the researcher to conduct fractal analysis and still complete field trials with final yield evaluation.     

菜豆根构型对低磷胁迫的适应性变化及基因型差异

利用特殊设计的营养袋纸培养和分层式磷控释砂培等根系生长系统结合计算机图像分析技术,以基根根长在生长介质各层的相对分布和基根平均生长角度为指标,定量测定菜豆（Ｐｈａｓｅｏｌｕｓ ｖｕｌｇａｒｉｓ Ｌ．）根构型在低磷胁迫下的适应性变化及其与磷效率的关系。结果表明,菜豆根构型对低磷胁迫具有适应性反应,在缺磷条件下基根向地性减弱,基根在生长介质表层相对分布增多、基根平均生长角度（与水平线夹角）变小,从而导     

Adaptive Changes and Genotypic Variation for Root Architecture of Common Bean in Response to Phosphorus Deficiency

Root architectural responses to phosphorus (p) availability may be an important trait for P acquisition efficiency. In the present study, The authors examined the effects of P availability on root architectural responses of different common bean genotypes. Five common bean (Phaseolus vulgaris L.) genotypes representing different origins and ecotypic races were compared both in a specially designed paper pouch system and a stratified P buffer sand culture system with computer image analysis. The results showed that root architecture was regulated by P availability. P deficiency led to form a shallower root system, as indicated by increased relative distribution of basal root length in the upper layers and decreased the growth angle of basal roots. There was significant genetic variation in root architecture in response to P deficiency both in the paper pouch system and the stratified sand culture system. Under low P conditions some genotypes were more gravitropically sensitive to low P availability, resulting in producing a shallower root system and enhanced root exploration into the surface soil, where soil available P is more concentrated. G19833 and DOR364, which were most contrasting in P efficiency, were also very different in root architectural response to P availability. The results from this study suggest that P availability regulates root architecture and P deficiency leads to shallower root architecture in beans. The genetic potential of root architecture provides the possibility of selecting this trait for improving P acquisition efficiency in common bean.     

Nitrogen fixation and plant growth of common bean (Phaseolus vulgaris L.) at different levels of phosphorus availability

The efficacy of the alumina system for differentiating between bean (Phaseolus vulgaris L.) genotypes for growth at different levels of phosphorus availability was determinated. In addition to response to P levels, comparisons were made between plants receiving N either from fertilizer or nitrogen fixation. When the cv. Carioca was provided with either 100 ppm of N or inoculated withRhizobium leguminosarum biovarphaseoli, differences in shoot dry weight and nodule number were related to P level. There was a greater proportion of green, ineffectivevs. red, active nodules at the low P concentration than at the higher P concentration. In a second experiment, two cvs., Puebla 152 and Carioca and the breeding line UW 24-21, either were inoculated with rhizobia or provided with 150ppm of N. Each genotype-nitrogen combination was grown at 8 levels of P. There was a positive effect of P level on shoot dry weight, nodule number and nodule mass. Root mass was affected less than nodule or shoot mass by the P level of the growth medium. Nodule mass, but not P concentration in the nodules, was affected by P level, whereas in the other plant tissues, P concentrations were lower at lower P levels in the media.     

Regulation of root hair density by phosphorus availability in Arabidopsis thaliana

We characterized the response of root hair density to phosphorus (P) availability in Arabidopsis thaliana. Arabidopsis plants were grown aseptically in growth media with varied phosphorus concentrations, ranging from 1 mmol m⁻³ to 2000 mmol m⁻³ phosphorus. Root hair density (number of root hairs per mm of root length) was analysed starting at 7 d of growth. Root hair density was highly regulated by phosphorus availability, increasing significantly in roots exposed to low-phosphorus availability. The initial root hairs produced by the radicle were not sensitive to phosphorus availability, but began to respond after 9 d of growth. Root hair density was about five times greater in low phosphorus (1 mmol m⁻³) than in high phosphorus (1000 mmol m⁻³) media. Root hair density decreased logarithmically in response to increasing phosphorus concentrations within that range. Root hair density also increased in response to deficiencies of several other nutrients, but not as strongly as to low phosphorus. Indoleacetic acid (IAA), the auxin transport inhibitor 2-(p-chlorophenoxy)-2-methylpropionic acid (CMPA), the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), and the ethylene synthesis inhibitor amino-oxyacetic acid (AOA) all increased root hair density under high phosphorus but had very little effect under low phosphorus. Low phosphorus significantly changed root anatomy, causing a 9% increase in root diameter, a 31% decrease in the cross-sectional area of individual trichoblasts, a 40% decrease in the cross-sectional area of individual atrichoblasts, and 45% more cortical cells in cross-section. The larger number of cortical cells and smaller epidermal cell size in low phosphorus roots increased the number of trichoblast files from eight to 12. Two-thirds of increased root hair density in low phosphorus roots was caused by increased likelihood of trichoblasts to form hairs, and 33% of the increase was accounted for by changes in low phosphorus root anatomy resulting in an increased number of trichoblast files. These results show that phosphorus availability can fundamentally alter root anatomy, leading to changes in root hair density, which are presumably important for phosphorus acquisition.     

Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris

Root architectural plasticity might be an important factor in the acquisition by plants of immobile nutrients such as phosphorus (P). In this study, we examined the effect of P availability on the orientation of basal roots with respect to gravity, and thereby on the growth angle of these roots of common bean (Phaseolus vulgaris L.). In one set of studies the growth angle of basal roots of bean seedlings was measured over time. Sixteen bean genotypes were examined; six showed a decrease in root orientation with respect to gravity in low P media, one increased orientation, and nine showed no difference within 5 d of basal root emergence. Bean taproots also showed decreased root orientation with respect to gravity in low P. Growth angle after 5 d was correlated with field performance of contrasting genotypes in low P tropical soils. Mineral deficiencies other than P did not cause changes in root angle. In a split pouch system that provided high or low P solution to different parts of the root system, the decrease in root angle in low P was found to be a response to global P availability, and not local to the portion of the root system in low P. Effects of P availability on root angle were associated with reduced shoot P concentration, but preceded effects on plant biomass accumulation and leaf area expansion. Results from growth pouches for genotype G 19833 were confirmed using a solid-phase buffered sand-culture system supplying P at three levels. Pea (Pisum sativum), soybean (Glycine max Williams), chickpea (Cicer arietinum), lima bean (Phaseolus lunatus), and lentil (Lens culinaris) were grown with and without P; soybean and pea also showed decreased basal root angles in low P.     

Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability

Low phosphorus availability stimulates root hair elongation in many plants, which may have adaptive significance in soil phosphorus acquisition. We investigated the effect of low phosphorus on the elongation of Arabidopsis thaliana root hairs. Arabidopsis thaliana plants were grown in plant culture containing high (1000 mmol m^?3) or low (1 mmol m^?3) phosphorus concentrations, and root hair elongation was analysed by image analysis. After 15d of growth, low-phosphorus plants developed root hairs averaging 0.9 mm in length while high-phosphorus plants of the same age developed root hairs averaging 0.3 mm in length. Increased root hair length in low-phosphorus plants was a result of both increased growth duration and increased growth rate. Root hair length decreased logarithmically in response to increasing phosphorus concentration. Local changes in phosphorus availability influenced root hair growth regardless of the phosphorus status of the plant. Low phosphorus stimulated root hair elongation in the hairless axr2 mutant, exogenously applied IAA stimulated root hair elongation in wild-type high-phosphorus plants and the auxin antagonist CM PA inhibited root hair elongation in low-phosphorus plants. These results indicate that auxin may be involved in the low-phosphorus response in root hairs.     

不同磷水平下小麦-蚕豆间作根系形态的变化及其与内源激素的关系

采用水培方法,研究了不同磷水平下小麦-蚕豆间作体系根系形态变化及其与内源激素的相关关系。结果表明: 与单作小麦相比,在低磷(1/2P)水平下,小麦-蚕豆间作能显著增加小麦的根长,显著减少小麦根系的平均直径,显著增加根系的表面积;在常规磷(P)水平下,间作能显著降低小麦根系的平均直径,有增加小麦根长和根表面积的趋势;与单作蚕豆相比,间作能明显促进蚕豆根系的增长,同时增加蚕豆根表面积。在1/2P水平下,间作能显著提高小麦和蚕豆根系中的生长素(IAA)、脱落酸(ABA)、水杨酸(SA)和茉莉酸(JA)含量;在P水平下,间作能显著提高小麦根系中的IAA、ABA和JA含量,单、间作小麦根系中的SA含量没有显著差异,间作显著增加了蚕豆根系中ABA和SA含量,单、间作蚕豆根系中的IAA和JA含量无显著差异。单作条件下,小麦和蚕豆根系中的内源激素(IAA、ABA、SA和JA)含量与其根系形态(根长、根平均直径和根表面积)无显著相关性;间作条件下,小麦和蚕豆根系中的IAA含量与根长和根表面积之间存在明显的正相关关系。由此可见,小麦-蚕豆间作能够诱导小麦和蚕豆根系IAA的增加。这种变化可能是驱动间作系统根系形态变化的重要因子。     

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.     

Responses of root architecture development to low phosphorus availability: a review

Background

Phosphorus (P) is an essential element for plant growth and development but it is often a limiting nutrient in soils. Hence, P acquisition from soil by plant roots is a subject of considerable interest in agriculture, ecology and plant root biology. Root architecture, with its shape and structured development, can be considered as an evolutionary response to scarcity of resources.

Scope

This review discusses the significance of root architecture development in response to low P availability and its beneficial effects on alleviation of P stress. It also focuses on recent progress in unravelling cellular, physiological and molecular mechanisms in root developmental adaptation to P starvation. The progress in a more detailed understanding of these mechanisms might be used for developing strategies that build upon the observed explorative behaviour of plant roots.

Conclusions

The role of root architecture in alleviation of P stress is well documented. However, this paper describes how plants adjust their root architecture to low-P conditions through inhibition of primary root growth, promotion of lateral root growth, enhancement of root hair development and cluster root formation, which all promote P acquisition by plants. The mechanisms for activating alterations in root architecture in response to P deprivation depend on changes in the localized P concentration, and transport of or sensitivity to growth regulators such as sugars, auxins, ethylene, cytokinins, nitric oxide (NO), reactive oxygen species (ROS) and abscisic acid (ABA). In the process, many genes are activated, which in turn trigger changes in molecular, physiological and cellular processes. As a result, root architecture is modified, allowing plants to adapt effectively to the low-P environment. This review provides a framework for understanding how P deficiency alters root architecture, with a focus on integrated physiological and molecular signalling.     

小麦与蚕豆间作体系根系形态与磷吸收的定量解析

豆科与禾本科作物间作能够改变作物根系生长,但不同施磷水平下间作-根系形态-磷吸收之间的关系尚未明确.本研究通过田间定位试验和根箱模拟试验,研究不同种植模式(小麦单作、蚕豆单作和小麦-蚕豆间作)和不同磷水平下小麦和蚕豆的产量、生物量、磷吸收及根系形态特征,分析探讨不同施磷条件下小麦-蚕豆间作对根系形态和磷吸收的影响.结果...     

Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems

Climate is predicted to change over the 21st century. However, little is known about how climate change can affect soil phosphorus (P) cycle and availability in global terrestrial ecosystems, where P is a key limiting nutrient. With a global database of Hedley P fractions and key‐associated physiochemical properties of 760 (seminatural) natural soils compiled from 96 published studies, this study evaluated how climate pattern affected soil P cycle and availability in global terrestrial ecosystems. Overall, soil available P, indexed by Hedley labile inorganic P fraction, significantly decreased with increasing mean annual temperature (MAT) and precipitation (MAP). Hypothesis‐oriented path model analysis suggests that MAT negatively affected soil available P mainly by decreasing soil organic P and primary mineral P and increasing soil sand content. MAP negatively affected soil available P both directly and indirectly through decreasing soil primary mineral P; however, these negative effects were offset by the positive effects of MAP on soil organic P and fine soil particles, resulting in a relatively minor total MAP effect on soil available P. As aridity degree was mainly determined by MAP, aridity also had a relatively minor total effect on soil available P. These global patterns generally hold true irrespective of soil depth (≤10 cm or >10 cm) or site aridity index (≤1.0 or >1.0), and were also true for the low‐sand (≤50%) soils. In contrast, available P of the high‐sand (>50%) soils was positively affected by MAT and aridity and negatively affected by MAP. Our results suggest that temperature and precipitation have contrasting effects on soil P availability and can interact with soil particle size to control soil P availability.     

Influence of ethylene on adventitious root formation in mung bean hypocotyl cuttings

The relationship between ethylene and adventitious root formation in mung bean hypocotyl cuttings was studied.Ethephon, an ethylene-releasing compound, at 5 x 10 -5 M increased root number and root dry weight on hypo-cotyl cuttings. When ethephon was applied to hypocotyl at different times after excision, there were two effectivetimes for root production i.e. between 06 h and 18-24 h. These two time periods correspond to the induction phase and the late initiation phase of root development, respectively. After excision, three peaks of ethylene productionwere observed. The first peak commencing at 6 h started the sequence of reactions leading root formation, the second peak appearing at 12 h coincided with the beginning of the increase of the IAA level during primordia initiation, and the third peak showing at 48 h played a role in root differentiation and growth. Ethylene stimulated rooting by enhancing the increase in auxins. Thus it appears that the IAA-induced ethylene production may be a factor involved in the stimulation of adventitious root formation.     

Microsatellite markers for the common bean Phaseolus vulgaris

Efforts to develop molecular tools for genetic analysis and breeding of common bean in the tropics are still limited. The number of microsatellite markers available for the crop is small compared to other crops of similar social and economic importance. As part of a project to broaden the use of molecular tools in bean breeding, a genomic library enriched for AG/TC repeat sequences was constructed for Phaseolus vulgaris. Twenty microsatellite markers were initially developed and 10 were characterized using a panel of 85 representative accessions of the bean gene bank. The number of alleles per marker ranged from three to 10. The polymorphism information content (PIC) varied from 0.23 to 0.80. The results indicate that the new markers can be readily used in genetically analysis of common bean.     

Soil moisture and potassium affect the performance of symbiotic nitrogen fixation in faba bean and common bean

Potassium (K) is reported to improve plant's resistance against environmental stress. A frequently experienced stress for plants in the tropics is water shortage. It is not known if sufficient K supply would help plants to partially overcome the effects of water stress, especially that of symbiotic nitrogen fixation which is often rather low in the tropics when compared to that of temperate regions. Thus, the impact of three levels of fertilizer potassium (0.1, 0.8 and 3.0 mM K) on symbiotic nitrogen fixation was evaluated with two legumes under high (field capacity to 25% depletion) and low (less than 50% of field capacity) water regimes. Plants were grown in single pots in silica sand under controlled conditions with 1.5 mM N (¹⁵N enriched NH₄NO₃). The species were faba bean (Vicia faba L.), a temperate, amide producing legume and common bean (Phaseolus vulgaris L.), a tropical, ureide producing species. In both species, 0.1 mM K was insufficient for nodulation at both moisture regimes, although plant growth was observed. The supply of 0.8 or 3.0 mM K allowed nodulation and subsequent nitrogen fixation which appeared to be adequate for respective plant growth. High potassium supply had a positive effect on nitrogen fixation, on shoot and root growth and on water potential in both water regimes. Where nodulation occurred, variations caused by either K or water supply had no consequences on the percentage of nitrogen derived from the symbiosis. The present data indicate that K can apparently alleviate water shortage to a certain extent. Moreover it is shown that the symbiotic system in both faba bean and common bean is less tolerant to limiting K supply than plants themselves. However, as long as nodulation occurs, N assimilation from the symbiotic source is not selectively affected by K as opposed to N assimilation from fertilizer.