Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium

Root cortical aerenchyma (RCA) is induced by hypoxia, drought, and several nutrient deficiencies. Previous research showed that RCA formation reduces the respiration and nutrient content of root tissue. We used SimRoot, a functional-structural model, to provide quantitative support for the hypothesis that RCA formation is a useful adaptation to suboptimal availability of phosphorus, nitrogen, and potassium by reducing the metabolic costs of soil exploration in maize (Zea mays). RCA increased the growth of simulated 40-d-old maize plants up to 55%, 54%, or 72% on low nitrogen, phosphorus, or potassium soil, respectively, and reduced critical fertility levels by 13%, 12%, or 7%, respectively. The greater utility of RCA on low-potassium soils is associated with the fact that root growth in potassium-deficient plants was more carbon limited than in phosphorus- and nitrogen-deficient plants. In contrast to potassium-deficient plants, phosphorus- and nitrogen-deficient plants allocate more carbon to the root system as the deficiency develops. The utility of RCA also depended on other root phenes and environmental factors. On low-phosphorus soils (7.5 μM), the utility of RCA was 2.9 times greater in plants with increased lateral branching density than in plants with normal branching. On low-nitrate soils, the utility of RCA formation was 56% greater in coarser soils with high nitrate leaching. Large genetic variation in RCA formation and the utility of RCA for a range of stresses position RCA as an interesting crop-breeding target for enhanced soil resource acquisition.     

Topsoil foraging – an architectural adaptation of plants to low phosphorus availability

Low phosphorus availability is a primary constraint to plant productivity in many natural and agricultural ecosystems. Plants display a wide array of adaptive responses to low phosphorus availability that generally serve to enhance phosphorus mobility in the soil and increase its uptake. One set of adaptive responses is the alteration of root architecture to increase phosphorus acquisition from the soil at minimum metabolic cost. In a series of studies with the common bean, work in our laboratory has shown that architectural traits that enhance topsoil foraging appear to be particularly important for genotypic adaptation to low phosphorus soils (phosphorus efficiency). In particular, the gravitropic trajectory of basal roots, adventitious rooting, the dispersion of lateral roots, and the plasticity of these processes in response to phosphorus availability contribute to phosphorus efficiency in this species. These traits enhance the exploration and exploitation of shallow soil horizons, where phosphorus availability is greatest in many soils. Studies with computer models of root architecture show that root systems with enhanced topsoil foraging acquire phosphorus more efficiently than others of equivalent size. Comparisons of contrasting genotypes in controlled environments and in the field show that plants with better topsoil foraging have superior phosphorus acquisition and growth in low phosphorus soils. It appears that many architectural responses to phosphorus stress may be mediated by the plant hormone ethylene. Genetic mapping of these traits shows that they are quantitatively inherited but can be tagged with QTLs that can be used in plant breeding programs. New crop genotypes incorporating these traits have substantially improved yield in low phosphorus soils, and are being deployed in Africa and Latin America.     

Mapping of QTL controlling root hair length in maize (<Emphasis Type="Italic">Zea mays</Emphasis> L.) under phosphorus deficiency

Suboptimal phosphorus availability is a primary constraint for terrestrial plant growth and crop productivity. Root hairs are subcellular extensions from the root epidermis that play an important role in the uptake of immobile nutrients such as phosphorus by increasing soil exploration. The objective of this study was to identify quantitative trait loci for root hair length and plasticity in response to phosphorus stress in maize. Using a cigar roll culture system in a controlled environment, root traits including root hair length, tap root length, root thickness, and root biomass were evaluated in 169 recombinant inbred lines derived from a cross between B73 and Mo17. These parents have contrasting adaptation to low phosphorus availability in the field. The parents segregated for the length of individual root hairs under low phosphorus. Average root hair length (RHL) of RI lines ranged from 0.6 to 3.5 mm with an average of 2.0 mm under fertile conditions, and RHL was increased from 0% to 185% under phosphorus stress. Using composite interval mapping with a LOD threshold of 3.27, one QTL was associated with RHL plasticity, three QTL with RHL under high fertility, and one QTL with root hair length under low phosphorus. These QTL accounted for 12.7%, 31.9%, and 9.6% of phenotypic variation, respectively. No QTL were detected for taproot thickness and root biomass. Six QTL were associated with 53.1% of the total variation for seed phosphorus in the population. Root biomass plasticity was significantly correlated with RHL induced by low phosphorus, taproot length plasticity, and seed phosphorus reserves. Our results suggest that genetic variation in root hair length and plasticity may be an appropriate target for marker aided selection to improve the phosphorus efficiency of maize.     

Improving crop nutrient efficiency through root architecture modifications

Improving crop nutrient ef ficiency becomes an essential consideration for environmentally friendly and sustainable agriculture. Plant growth and development is dependent on 17 essential nutrient elements,among them,nitrogen(N) and phosphorus(P) are the two most important mineral nutrients. Hence it is not surprising that low N and/or low P availability in soils severely constrains crop growth and productivity,and thereby have become high priority targets for improving nutrient ef ficiency in crops. Root exploration largely determines the ability of plants to acquire mineral nutrients from soils. Therefore,root architecture,the 3-dimensional con figuration of the plant's root system in the soil,is of great importance for improving crop nutrient ef ficiency. Furthermore,the symbiotic associations between host plants and arbuscular mycorrhiza fungi/rhizobial bacteria,are additional important strategies to enhance nutrient acquisition. In this review,we summarize the recent advances in the current understanding of crop species control of root architecture alterations in response to nutrient availability and root/microbe symbioses,through gene or QTL regulation,which results in enhanced nutrient acquisition.     

植物根构型特性与磷吸收效率

植物根构型,即根系在生长介质中的空间造型和分布,与磷吸收效率密切相关;认识植物根构型,可为植物磷效率的遗传改良提供依据。长期以来,人们试图定量描述植物根构型,确立一个能客观全面地描述根系三维立体构型的综合指标。试验指出,植物主要通过向地性变化和根冠之间的碳源分配来改变根构型,从而影响磷吸收效率;根系向地性变化可由缺磷等因素所诱导,且存在着一定的遗传变异性。有证据表明,根构型对低磷胁迫的适应性变化是     

The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes

A common response to low phosphorus availability is increased relative biomass allocation to roots. The resulting increase in root:shoot ratio presumably enhances phosphorus acquisition, but may also reduce growth rates by diverting carbon to the production of heterotrophic rather than photosynthetic tissues. To assess the importance of increased carbon allocation to roots for the adaptation of plants to low P availability, carbon budgets were constructed for four common bean genotypes with contrasting adaptation to low phosphorus availability in the field ("phosphorus efficiency"). Solid-phase-buffered silica sand provided low (1 microM), medium (10 microM), and high (30 microM) phosphorus availability. Compared to the high phosphorus treatment, plant growth was reduced by 20% by medium phosphorus availability and by more than 90% by low phosphorus availability. Low phosphorus plants utilized a significantly larger fraction of their daytime net carbon assimilation on root respiration (c. 40%) compared to medium and high phosphorus plants (c. 20%). No significant difference was found among genotypes in this respect. Genotypes also had similar rates of P absorption per unit root weight and plant growth per unit of P absorbed. However, P-efficient genotypes allocated a larger fraction of their biomass to root growth, especially under low P conditions. Efficient genotypes had lower rates of root respiration than inefficient genotypes, which enabled them to maintain greater root biomass allocation than inefficient genotypes without increasing overall root carbon costs.     

Root traits as tools for creating phosphorus efficient crop varieties

This paper provides a brief assessment of the genetic variation in root properties (root morphology, including root hairs), mycorrhizal symbiosis, uptake kinetics parameters and root-induced changes (pH, organic acids and acid phosphatase) in the rhizosphere of various crop species and their genotypes and then briefly discusses the opportunities and challenges of using such knowledge for enhancing P efficiency of future crop genotypes by genetic means. Wide genotypic variation and heritability of root morphology, root hair length and density and thereby P acquisition provide opportunities for selection and breeding for root characteristics for increasing P acquisition. The progress is challenged by the concerns of high carbon cost of larger root systems and by the lack of cost effective methods to determine root length of a large number of genotypes under field conditions. The carbon cost of root hairs is low. Furthermore, low cost methods now exist to compare root hair formation of field grown genotypes. The development and application of sophisticated methods has advanced our knowledge on the role of mycorrhizal symbiosis in P acquisition and also on the molecular basis of fungi and plant interactions. However, extensive studies to explore genotypic variation in mycorrhizal responsiveness are rare, which makes it difficult to assess, how mycorrhizal symbiosis can be manipulated through breeding efforts. The promising variation found in P uptake kinetics parameters of crop genotypes in few studies indicates that more genotypes may be screened by relatively simple nutrient solution culture techniques. The genetic manipulation of the overall differences in cation-anion uptake, which is the main cause of rhizosphere pH change, may be difficult. For manipulation of rhizosphere pH, agronomic measures such as applications of ammonium or nitrate fertilisers may be more useful than breeding approaches. Also it seems difficult to assess what kind of genetic analysis should be performed to support the breeding efforts. Phosphorus mobilisation effect of pH depends on soil P compounds, therefore will differ with soil type. Both the enhanced release of organic acids and higher acid phosphatase activity in the rhizosphere may be useful for increasing P acquisition from inorganic and organic P pools, respectively. Modification of these traits by genetic means should be considered. For successful breeding programmes, the role of various root traits needs to be targeted in an integrated manner and then methods need to be developed for studying their importance under natural soil conditions, so that the genotypic variation can be explored and their ecological significance in P acquisition can be established.     

Cluster Roots: A Curiosity in Context

Cluster roots are an adaptation for nutrient acquisition from nutrient-poor soils. They develop on root systems of a range of species belonging to a number of different families (e.g., Proteaceae, Casuarinaceae, Fabaceae and Myricaceae) and are also found on root systems of some crop species (e.g., albus, Macadamia integrifoliaandCucurbita pepo). Their morphology is variable but typically, large numbers of determinate branch roots develop over very short distances of main root axes. Root clusters are ephemeral, and continually replaced by extension of the main root axes. Carboxylates are released from cluster roots at very fast rates for only a few days during a brief developmental window termed an ‘exudative burst’. Most of the studies of cluster-root metabolism have been carried out using the crop plant L. albus, but results on native plants have provided important additional information on carbon metabolism and exudate composition. Cluster-root forming species are generally non-mycorrhizal, and rely upon their specialised roots for the acquisition of phosphorus and other scarcely available nutrients. Phosphorus is a key plant nutrient for altering cluster-root formation, but their formation is also influenced by N and Fe. The initiation and growth of cluster roots is enhanced when plants are grown at a very low phosphate supply (viz. ≤1 μM P), and cluster-root suppression occurs at relatively higher P supplies. An important feature of some Proteaceae is storage of phosphorus in stem tissues which is associated with the seasonality of cluster-root development and P uptake (winter) and shoot growth (summer), and also maintains low leaf [P]. Some species of Proteaceae develop symptoms of P toxicity at relatively low external P supply. Our findings with Hakea prostrata (Proteaceae) indicate that P-toxicity symptoms result after the capacity of tissues to store P is exceeded. P accumulation in H. prostrata is due to its strongly decreased capacity to down-regulate P uptake when the external P supply is supra-optimal. The present review investigates cluster-root functioning in (1) L.albus (white lupin), the model crop plant for cluster-root studies, and (2) native Proteaceae that have evolved in phosphate-impoverished environments.     

亚热带6个典型树种吸收细根寿命与形态属性格局

根周转是地下生态过程的主要驱动力, 根属性指征了物种生态策略, 根寿命与属性是理解生态系统碳氮循环和群落多样性的关键。目前对亚热带常绿阔叶林根周转等生态过程的直接观测资料缺乏。该研究对中亚热带江西樟树试验林场6个树种吸收细根动态进行了2年观测, 获取了2.8万张微根管照片, 分析了吸收细根寿命年际和季节变化特征及其与根形态属性的关系。结果显示: 1)亚热带6个树种间吸收细根寿命变异为4.6倍, 变异系数可达73%。中值寿命排序为: 红豆杉(Taxus wallichiana)(426天) >复羽叶栾树( Koelreuteria bipinnata)(155天) >竹柏( Nageia nagi)(145天) >樟( Cinnamomum camphora)(126天) >东京樱花( Cerasus yedoensis)(93天) >深山含笑( Michelia maudiae)(92天); 2)树木吸收细根寿命年际、季节变异较大, 可能是适应伏秋旱、雨热不同期、年际变化大的亚热带季风气候的结果; 3)吸收细根寿命与直径呈显著正相关关系, 与比根长呈显著负相关关系, 表明根的构建成本可以在一定程度上预测寿命。这些结果为预测亚热带地下生态过程、揭示亚热带常绿阔叶林碳氮循环、物种共存机制提供依据。     

Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.)

Root cortical aerenchyma (RCA) reduces root respiration in maize by converting living cortical tissue to air volume. We hypothesized that RCA increases drought tolerance by reducing root metabolic costs, permitting greater root growth and water acquisition from drying soil. To test this hypothesis, recombinant inbred lines with high and low RCA were observed under water stress in the field and in soil mesocosms in a greenhouse. In the field, lines with high RCA had 30% more shoot biomass at flowering compared with lines with low RCA under water stress. Root length density in deep soil was significantly greater in the high RCA lines compared with the low RCA lines. Mid‐day leaf relative water content in the high RCA lines was 10% greater than in the low RCA lines under water stress. The high RCA lines averaged eight times the yield of the low RCA lines under water stress. In mesocosms, high RCA lines had less seminal root respiration, deeper rooting, and greater shoot biomass compared with low RCA lines under water stress. These results support the hypothesis that RCA is beneficial for drought tolerance in maize by reducing the metabolic cost of soil exploration.     

亚热带典型树种根毛特征及其与共生真菌的关系

根毛和共生真菌增加了吸收面积,提高了植物获取磷等土壤资源的能力。由于野外原位观测根表微观结构较为困难,吸收细根、根毛、共生真菌如何相互作用并适应土壤资源供应,缺乏相应的数据和理论。该研究以受磷限制的亚热带森林为对象,选取了21种典型树种,定量了根毛存在情况、属性变异,分析了根毛形态特征与共生真菌侵染率、吸收细根功能属性之间的关系,探讨了根表结构对低磷土壤的响应和适应格局。结果表明:1)在亚热带森林根毛不是普遍存在的, 21个树种中仅发现7个树种存有根毛, 4个为丛枝菌根(AM)树种, 3个为外生菌根(ECM)树种。其中,马尾松(Pinus massoniana)根毛出现率最高,为86%;2)菌根类型是理解根-根毛-共生真菌关系的关键,AM树种根毛密度与共生真菌侵染率正相关,但ECM树种根毛直径与共生真菌侵染率负相关; 3) AM树种根毛长度和根毛直径、ECM树种根毛出现率与土壤有效磷含量呈负相关关系。该研究揭示了不同菌根类型树种根毛-共生真菌-根属性的格局及相互作用,为精细理解养分获取策略奠定了基础。     

植物根构型特性与磷吸收效率

植物根构型，即根系在生长介质中的空间造型和分布，与磷吸收效率密切相关；认识植物根构型，可为植物磷效率的遗传改良提供依据。长期以来，人们试图定量描述植物根构型，确立一个能客观全面地描述根系三维立体构型的综合指标。试验指出，植物主要通过向地性变化和根冠之间的碳源分配来改变根构型, 从而影响磷吸收效率；根系向地性变化可由缺磷等因素所诱导，且存在着一定的遗传变异性。有证据表明，根构型对低磷胁迫的适应性变化是受基因调控的一个生理过程，其中乙烯可能是一种重要的生理调节物质。迄今已在一些植物上定位到了部分控制根构型的数量性状座位，为该性状的分子生物学改良提供了基础。随着现代技术的进展，植物根构型研究将取得更大的突破。     

Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding

Background

Rice is the world''s most important cereal crop and phosphorus (P) and zinc (Zn) deficiency are major constraints to its production. Where fertilizer is applied to overcome these nutritional constraints it comes at substantial cost to farmers and the efficiency of fertilizer use is low. Breeding crops that are efficient at acquiring P and Zn from native soil reserves or fertilizer sources has been advocated as a cost-effective solution, but would benefit from knowledge of genes and mechanisms that confer enhanced uptake of these nutrients by roots.

Scope

This review discusses root traits that have been linked to P and Zn uptake in rice, including traits that increase mobilization of P/Zn from soils, increase the volume of soil explored by roots or root surface area to recapture solubilized nutrients, enhance the rate of P/Zn uptake across the root membrane, and whole-plant traits that affect root growth and nutrient capture. In particular, this review focuses on the potential for these traits to be exploited through breeding programmes to produce nutrient-efficient crop cultivars.

Conclusions

Few root traits have so far been used successfully in plant breeding for enhanced P and Zn uptake in rice or any other crop. Insufficient genotypic variation for traits or the failure to enhance nutrient uptake under realistic field conditions are likely reasons for the limited success. More emphasis is needed on field studies in mapping populations or association panels to identify those traits and underlying genes that are able to enhance nutrient acquisition beyond the level already present in most cultivars.     

Root carbon and protein metabolism associated with heat tolerance

Extensive past efforts have been taken toward understanding heat tolerance mechanisms of the aboveground organs. Root systems play critical roles in whole-plant adaptation to heat stress, but are less studied. This review discusses recent research results revealing some critical physiological and metabolic factors underlying root thermotolerance, with a focus on temperate perennial grass species. Comparative analysis of differential root responses to supraoptimal temperatures by a heat-adapted temperate C3 species, Agrostis scabra, which can survive high soil temperatures up to 45 °C in geothermal areas in Yellow Stone National Park, and a heat-sensitive cogeneric species, Agrostis stolonifera, suggested that efficient carbon and protein metabolism is critical for root thermotolerance. Superior root thermotolerance in a perennial grass was associated with a greater capacity to control respiratory costs through respiratory acclimation, lowering carbon investment in maintenance for protein turnover, and efficiently partitioning carbon into different metabolic pools and alternative respiration pathways. Proteomic analysis demonstrated that root thermotolerance was associated with an increased maintenance of stability and less degradation of proteins, particularly those important for metabolism and energy production. In addition, thermotolerant roots are better able to maintain growth and activity during heat stress by activating stress defence proteins such as those participating in antioxidant defence (i.e. superoxide dismutase, peroxidase, glutathione S-transferase) and chaperoning protection (i.e. heat shock protein).     

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.     

放牧影响下典型草原克氏针茅和多根葱根系属性比较

植物根系属性与其生态适应性密切相关.为明确不同放牧干扰下克氏针茅和多根葱两种优势植物根系属性差异,比较了轻度放牧、中度放牧、重度放牧下克氏针茅和多根葱地下根系长度、根系表面积、根系直径、根系体积、根尖数、根系分叉数、比根长和比表面积的形态特征,分析了2种植物根尖比、根长比、表面积比、体积比等根系形态格局,研究两种植物对...     

常绿阔叶林外生和丛枝菌根树种细根形态和构型性状对氮添加的可塑性响应

以中亚热带常绿阔叶林外生菌根树种罗浮栲和丛枝菌根树种木荷为研究对象,采用根袋法进行野外原位氮添加试验,研究了细根形态性状(比根长、比表面积、组织密度、平均根直径)和构型性状(分枝数、分枝比、根长增长速率、根尖密度、分枝密度),分析不同菌根树种细根形态和构型性状对氮沉降的响应.结果表明:随序级增加,外生和丛枝菌根树种细根...     

Linking root respiration to chemistry and morphology across species

Root respiration is a critical physiological trait involved in root resource acquisition strategies, yet it is less represented in root trait syndrome. Here we compiled a large dataset of root respiration associated with root chemical and morphological traits from 245 plant species. Our results demonstrated that root respiration correlated positively with root nitrogen concentration (RNC) and negatively with root tissue density (RTD) across and within woody and non‐woody species. However, the relationships between root respiration and specific root length (SRL) and root diameter (RD) were weak or even insignificant. Such root respiration–traits relationships were not completely in line with predictions by the root economics spectrum (RES). Furthermore, the principal component analysis showed that root trait syndrome was multidimensional. Root respiration was associated more strongly with the RNC‐RTD axis (the classical RES) than with the orthogonal SRL‐RD axis for woody species, but not for non‐woody species. Collectively, the linkages of root physiological, chemical, and morphological traits provide a better understanding of root trait covariation and root resource acquisition strategies.     

Engineering crop nutrient efficiency for sustainable agriculture

Increasing crop yields can provide food, animal feed, bioenergy feedstocks and biomaterials to meet increasing global demand; however, the methods used to increase yield can negatively affect sustainability. For example, application of excess fertilizer can generate and maintain high yields but also increases input costs and contributes to environmental damage through eutrophication, soil acidification and air pollution. Improving crop nutrient efficiency can improve agricultural sustainability by increasing yield while decreasing input costs and harmful environmental effects. Here, we review the mechanisms of nutrient efficiency (primarily for nitrogen, phosphorus, potassium and iron) and breeding strategies for improving this trait, along with the role of regulation of gene expression in enhancing crop nutrient efficiency to increase yields. We focus on the importance of root system architecture to improve nutrient acquisition efficiency, as well as the contributions of mineral translocation, remobilization and metabolic efficiency to nutrient utilization efficiency.     

Optimizing reproductive phenology in a two-resource world: a dynamic allocation model of plant growth predicts later reproduction in phosphorus-limited plants

Background and Aims

Timing of reproduction is a key life-history trait that is regulated by resource availability. Delayed reproduction in soils with low phosphorus availability is common among annuals, in contrast to the accelerated reproduction typical of other low-nutrient environments. It is hypothesized that this anomalous response arises from the high marginal value of additional allocation to root growth caused by the low mobility of phosphorus in soils.

Methods

To better understand the benefits and costs of such delayed reproduction, a two-resource dynamic allocation model of plant growth and reproduction is presented. The model incorporates growth, respiration, and carbon and phosphorus acquisition of both root and shoot tissue, and considers the reallocation of resources from senescent leaves. The model is parameterized with data from Arabidopsis and the optimal reproductive phenology is explored in a range of environments.

Key Results

The model predicts delayed reproduction in low-phosphorus environments. Reproductive timing in low-phosphorus environments is quite sensitive to phosphorus mobility, but is less sensitive to the temporal distribution of mortality risks. In low-phosphorus environments, the relative metabolic cost of roots was greater, and reproductive allocation reduced, compared with high-phosphorus conditions. The model suggests that delayed reproduction in response to low phosphorus availability may be reduced in plants adapted to environments where phosphorus mobility is greater.

Conclusions

Delayed reproduction in low-phosphorus soils can be a beneficial response allowing for increased acquisition and utilization of phosphorus. This finding has implications both for efforts to breed crops for low-phosphorus soils, and for efforts to understand how climate change may impact plant growth and productivity in low-phosphorus environments.