Metabolic Costs Of Soil Exploration Research Articles

Cortical parenchyma wall width regulates root metabolic cost and maize performance under suboptimal water availability.

We describe how increased root cortical parenchyma wall width (CPW) can improve tolerance to drought stress in maize by reducing the metabolic costs of soil exploration. Significant variation (1.0 to 5.0 µm) for CPW was observed in maize germplasm. The functional-structural model RootSlice predicts that increasing CPW from 2 to 4 µm is associated with ca. 15% reduction in root cortical cytoplasmic volume, respiration rate, and nitrogen content. Analysis of genotypes with contrasting CPW grown with and without water stress in the field confirms that increased CPW is correlated with ca. 32 to 42% decrease in root respiration. Under water stress in the field, increased CPW is correlated with 125% increased stomatal conductance, 325% increased leaf CO2 assimilation rate, 73 to 78% increased shoot biomass, and 92 to 108% increased yield. CPW was correlated with leaf mesophyll midrib parenchyma wall width, indicating pleiotropy. GWAS analysis identified candidate genes underlying CPW. OpenSimRoot modeling predicts that a reduction in root respiration due to increased CPW would also benefit maize growth under suboptimal nitrogen, which requires empirical testing. We propose CPW as a new phene that has utility under edaphic stress meriting further investigation.

Root phenotypes for improved nitrogen capture

Abstract Background Suboptimal nitrogen availability is a primary constraint for crop production in low-input agroecosystems, while nitrogen fertilization is a primary contributor to the energy, economic, and environmental costs of crop production in high-input agroecosystems. In this article we consider avenues to develop crops with improved nitrogen capture and reduced requirement for nitrogen fertilizer. Scope Intraspecific variation for an array of root phenotypes has been associated with improved nitrogen capture in cereal crops, including architectural phenotypes that colocalize root foraging with nitrogen availability in the soil; anatomical phenotypes that reduce the metabolic costs of soil exploration, improve penetration of hard soil, and exploit the rhizosphere; subcellular phenotypes that reduce the nitrogen requirement of plant tissue; molecular phenotypes exhibiting optimized nitrate uptake kinetics; and rhizosphere phenotypes that optimize associations with the rhizosphere microbiome. For each of these topics we provide examples of root phenotypes which merit attention as potential selection targets for crop improvement. Several cross-cutting issues are addressed including the importance of soil hydrology and impedance, phenotypic plasticity, integrated phenotypes, in silico modeling, and breeding strategies using high throughput phenotyping for co-optimization of multiple phenes. Conclusions Substantial phenotypic variation exists in crop germplasm for an array of root phenotypes that improve nitrogen capture. Although this topic merits greater research attention than it currently receives, we have adequate understanding and tools to develop crops with improved nitrogen capture. Root phenotypes are underutilized yet attractive breeding targets for the development of the nitrogen efficient crops urgently needed in global agriculture.

Root and Shoot Growth of a Modern and an Old Tall Durum Wheat (Triticum durum Desf.) Variety under Dual-Purpose Management.

In dual-purpose cereal systems, the co-production of fodder and grain can increase farm profitability and reduce farming risks. Our work evaluated shoot and root growth in durum wheat (Triticum durum Desf.) under dual-purpose management in a medium-high rainfall area of southern Italy. We compared a modern variety (Core) with a tall ancient variety (Saragolle lucana) under traditional (NDP) and dual-purpose (DP) management and tested the hypothesis that clipping plants during the vegetative stage would reduce root growth and dewatering before anthesis, which is advantageous in drought-prone environments. Experiments were conducted in Bella (PZ), Basilicata region, southern Italy (40°42' N, 15°32' E) on a clay loam soil in 2021 in a split-plot design on 2 × 2 main plots and 1 × 2 split-plots with 6 replicates. The DP treatment consisted of simulated grazing by clipping plants at 5 cm from the ground 3 months after sowing (at first hollow stem). Forage Biomass was not different at p = 0.05 between varieties, with an average of 0.58 t ha-1 DM. Grain yield was not penalized by clipping (p = 0.05) and did not differ significantly between varieties. SPAD was always lower in the Saragolle variety and lowered by clipping. Defoliation delayed phenology in both cultivars but did not reduce the final number of spikes per square meter. Stomatal conductance was correlated to temperature, did not differ between cultivars, and was not influenced by clipping. Soil water depletion was monitored in modern wheat from the booting stage to the beginning of grain filling. Clipping did not result in a reduction in pre-anthesis water depletion, possibly due to evaporative losses. Root density was markedly reduced by clipping in core variety between 0.20 and 0.60 m and much less in Saragolle. Unclipped Saragolle produced thicker roots and higher root masses compared to clipped plants. Defoliated Saragolle shifted to finer roots, reducing root mass more than length. This may have reduced the metabolic cost of soil exploration, thereby increasing root foraging efficiency.

Spatiotemporal responses of rice root architecture and anatomy to drought

AimsGrowth reductions and yield losses from drought could be mitigated by developing rice genotypes with more efficient root systems. We examined spatiotemporal responses to drought in order to determine whether roots developing in upper vs. deeper soil layers respond differently to drought stress.MethodsRoot anatomical and architectural phenotypes of two rice genotypes, Azucena (drought tolerant) and IR64 (drought susceptible), were measured weekly in well-watered and vegetative-stage drought stress treatments in solid medium with stratified moisture availability. Basal and apical segments were collected from older, deeper nodal roots and apical segments from younger, shallow roots for assessment of anatomy and lateral rooting phenotypes. The relationship between root anatomy and root respiration rates was tested in solution culture and solid medium.ResultsCompared to IR64, Azucena had deeper root systems and larger diameter roots in both treatments but reduced its living tissue area in response to drought, while IR64 roots exhibited less plasticity in root diameter. Root respiration rates were positively correlated with root diameter and living tissue area, providing evidence that root anatomy affects the metabolic cost of tissues. In response to drought, Azucena showed reduced theoretical axial hydraulic conductance in shallow roots and at the base of deep roots but slightly greater conductance at the tip of deep roots, while IR64 displayed low plasticity in metaxylem phenotypes.ConclusionWe propose that the plasticity of root phenotypes in Azucena contributes to its drought tolerance by reducing the metabolic cost of soil exploration and improving the efficiency of water transport.

Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize.

Root anatomical phenotypes vary among maize (Zea mays) cultivars and may have adaptive value by modifying the metabolic cost of soil exploration. However, the microbial trade-offs of these phenotypes are unknown. We hypothesized that nodal roots of maize with contrasting cortical anatomy have different patterns of mutualistic and pathogenic fungal colonization. Arbuscular mycorrhizal colonization in the field and mesocosms, root rots in the field, and Fusarium verticillioides colonization in mesocosms were evaluated in maize genotypes with contrasting root cortical anatomy. Increased aerenchyma and decreased living cortical area were associated with decreased mycorrhizal colonization in mesocosm and field experiments with inbred genotypes. In contrast, mycorrhizal colonization of hybrids increased with larger aerenchyma lacunae; this increase coincided with larger root diameters of hybrid roots. F. verticillioides colonization was inversely correlated with living cortical area in mesocosm-grown inbreds, and no relation was found between root rots and living cortical area or aerenchyma in field-grown hybrids. Root rots were positively correlated with cortical cell file number and inversely correlated with cortical cell size. Mycorrhizae and root rots were inversely correlated in field-grown hybrids. We conclude that root anatomy is associated with differential effects on pathogens and mycorrhizal colonization of nodal roots in maize.

Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture

Nutrient-efficient crops are a solution to the two grand challenges of modern agriculture: improving food security while reducing environmental impacts. The primary challenges are (1) nitrogen (N) and phosphorus (P) efficiency; (2) potassium (K), calcium (Ca), and magnesium (Mg) efficiency for acid soils; and (3) iron (Fe) and zinc (Zn) efficiency for alkaline soils. Root phenotypes are promising breeding targets for each of these. The Topsoil Foraging ideotype is beneficial for P capture and should also be useful for capture of K, Ca, and Mg in acid soils. The Steep, Cheap, and Deep ideotype for subsoil foraging is beneficial for N and water capture. Fe and Zn capture can be improved by targeting mechanisms of metal mobilization in the rhizosphere. Root hairs and phenes that reduce the metabolic cost of soil exploration should be prioritized in breeding programs. Nutrient-efficient crops should provide benefits at all input levels. Although our current understanding is sufficient to deploy root phenotypes for improved nutrient capture in crop breeding, this complex topic does not receive the resources it merits in either applied or basic plant biology. Renewed emphasis on these topics is needed in order to develop the nutrient-efficient crops urgently needed in global agriculture.

Does phosphorus deficiency induce formation of root cortical aerenchyma maintaining growth of Cunninghamia lanceolata?

Phosphorous (P) deficiency induces root cortical aerenchyma (RCA) formation in Chinese fir seedlings with marked genotypic variation, and the adaptive role of RCA is mainly related to root P reduction. Root cortical aerenchyma (RCA) formation in response to phosphorus (P) deficiency and its adaptive role are largely unexplored in trees. We hypothesized that RCA formation in response to P deficiency varies with its severity and genotype, and that P-stressed seedlings maintain similar seedling growth to non-stressed seedlings by reducing the P requirements of roots and metabolic cost of soil exploration. Seedlings of two half-sib families (nos. 25 and 36) of Cunninghamia lanceolata (Chinese fir) were grown in pots with three levels of P supply for 3 months. Significant differences in RCA formation in 40–45 mm root segments from the root tip were observed between families and P supply levels. Severe P deficiency induced more RCA formation in family no. 36 than in family no. 25, whereas moderate P deficiency induced RCA formation in family no. 36 only. Family no. 36 had significantly higher height increment, needle biomass, and P concentration in stems and needles, but lower root biomass and root P concentration, than family 25. A significantly negative relationship was found between RCA and root P concentration, increments in average root diameter, and root surface area, whereas significantly positive correlations were observed between some root morphological traits and biomass and P concentration in the organs of P-stressed seedlings of family 36. In conclusion, severe P deficiency induces formation of RCA in Chinese fir seedlings with marked genotypic variation, and the adaptive role of RCA formation during P deficiency is mainly related to the reduction of root P concentration.

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 0.2mm2 less LCA under low phosphorus had 75% less root segment respiration, 54% less root phosphorus content, rooted 20cm deeper, allocated up to four times more roots between 60 and 120cm 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.

Reduced Lateral Root Branching Density Improves Drought Tolerance in Maize.

An emerging paradigm is that root traits that reduce the metabolic costs of soil exploration improve the acquisition of limiting soil resources. Here, we test the hypothesis that reduced lateral root branching density will improve drought tolerance in maize (Zea mays) by reducing the metabolic costs of soil exploration, permitting greater axial root elongation, greater rooting depth, and thereby greater water acquisition from drying soil. Maize recombinant inbred lines with contrasting lateral root number and length (few but long [FL] and many but short [MS]) were grown under water stress in greenhouse mesocosms, in field rainout shelters, and in a second field environment with natural drought. Under water stress in mesocosms, lines with the FL phenotype had substantially less lateral root respiration per unit of axial root length, deeper rooting, greater leaf relative water content, greater stomatal conductance, and 50% greater shoot biomass than lines with the MS phenotype. Under water stress in the two field sites, lines with the FL phenotype had deeper rooting, much lighter stem water isotopic signature, signifying deeper water capture, 51% to 67% greater shoot biomass at flowering, and 144% greater yield than lines with the MS phenotype. These results entirely support the hypothesis that reduced lateral root branching density improves drought tolerance. The FL lateral root phenotype merits consideration as a selection target to improve the drought tolerance of maize and possibly other cereal crops.

Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.)

It has recently been shown that root cortical aerenchyma (RCA) formation substantially reduces the metabolic costs of soil exploration, thereby improving rooting depth, water capture, and plant growth under drought. The objectives of this study were to evaluate phenotypic variation of RCA formation in Malawi maize germplasm and confirm the utility of RCA formation in different agroecologies at field stations and on smallholder farms in Malawi. Forty maize accessions collected across Malawi were grown under rainfed field conditions, and a subset contrasting for RCA were grown under well-watered and water stressed conditions at two research stations and under natural drought on farms across two agroecological zones in Malawi. We found substantial variation for RCA in local germplasm ranging from 0% to 37% of root cross sectional area. Suboptimal water availability increased RCA from 54% to 77% across environments. Under water stress high RCA genotypes had 23% to 29% greater leaf relative water content, 67% to 96% greater shoot biomass 70 days after planting, and 78% to 143% greater grain yield than low RCA genotypes. Our results are consistent with the hypothesis that RCA improves plant growth under drought by reducing the metabolic costs of soil exploration and improving water acquisition. RCA has value as a selection criterion to improve the performance of maize and possibly other cereal crops in water limited environments.

Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture.

Crop genotypes with reduced metabolic costs of soil exploration would have improved water and nutrient acquisition. Three strategies to achieve this goal are (1) production of the optimum number of axial roots; (2) greater biomass allocation to root classes that are less metabolically demanding; and (3) reduction of the respiratory requirement of root tissue. An example of strategy 1 is the case of reduced crown root number in maize, which is associated with greater rooting depth, N capture and yield in low N soil. An example of strategy 2 is the case of increased hypocotyl-borne rooting in bean, which decreases root cost and increases P capture from low P soil. Examples of strategy 3 are the cases of increased formation of root cortical aerenchyma, decreased cortical cell file number and increased cortical cell size in maize, which decrease specific root respiration, increase rooting depth and increase water capture and yield under water stress. Root cortical aerenchyma also increases N capture and yield under N stress. Root phenes that reduce the metabolic cost of soil exploration are promising, underexploited avenues to the climate-resilient, resource-efficient crops that are urgently needed in global agriculture.

Reduced root cortical cell file number improves drought tolerance in maize.

We tested the hypothesis that reduced root cortical cell file number (CCFN) would improve drought tolerance in maize (Zea mays) by reducing the metabolic costs of soil exploration. Maize genotypes with contrasting CCFN were grown under well-watered and water-stressed conditions in greenhouse mesocosms and in the field in the United States and Malawi. CCFN ranged from six to 19 among maize genotypes. In mesocosms, reduced CCFN was correlated with 57% reduction of root respiration per unit of root length. Under water stress in the mesocosms, genotypes with reduced CCFN had between 15% and 60% deeper rooting, 78% greater stomatal conductance, 36% greater leaf CO2 assimilation, and between 52% to 139% greater shoot biomass than genotypes with many cell files. Under water stress in the field, genotypes with reduced CCFN had between 33% and 40% deeper rooting, 28% lighter stem water oxygen isotope enrichment (δ(18)O) signature signifying deeper water capture, between 10% and 35% greater leaf relative water content, between 35% and 70% greater shoot biomass at flowering, and between 33% and 114% greater yield than genotypes with many cell files. These results support the hypothesis that reduced CCFN improves drought tolerance by reducing the metabolic costs of soil exploration, enabling deeper soil exploration, greater water acquisition, and improved growth and yield under water stress. The large genetic variation for CCFN in maize germplasm suggests that CCFN merits attention as a breeding target to improve the drought tolerance of maize and possibly other cereal crops.

Large root cortical cell size improves drought tolerance in maize.

The objective of this study was to test the hypothesis that large cortical cell size (CCS) would improve drought tolerance by reducing root metabolic costs. Maize (Zea mays) lines contrasting in root CCS measured as cross-sectional area were grown under well-watered and water-stressed conditions in greenhouse mesocosms and in the field in the United States and Malawi. CCS varied among genotypes, ranging from 101 to 533 µm(2). In mesocosms, large CCS reduced respiration per unit of root length by 59%. Under water stress in mesocosms, lines with large CCS had between 21% and 27% deeper rooting (depth above which 95% of total root length is located in the soil profile), 50% greater stomatal conductance, 59% greater leaf CO2 assimilation, and between 34% and 44% greater shoot biomass than lines with small CCS. Under water stress in the field, lines with large CCS had between 32% and 41% deeper rooting (depth above which 95% of total root length is located in the soil profile), 32% lighter stem water isotopic ratio of (18)O to (16)O signature, signifying deeper water capture, between 22% and 30% greater leaf relative water content, between 51% and 100% greater shoot biomass at flowering, and between 99% and 145% greater yield than lines with small cells. Our results are consistent with the hypothesis that large CCS improves drought tolerance by reducing the metabolic cost of soil exploration, enabling deeper soil exploration, greater water acquisition, and improved growth and yield under water stress. These results, coupled with the substantial genetic variation for CCS in diverse maize germplasm, suggest that CCS merits attention as a potential breeding target to improve the drought tolerance of maize and possibly other cereal crops.

Root cortical burden influences drought tolerance in maize.

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. 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. 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. 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.

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.

Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability.

The formation of root cortical aerenchyma (RCA) reduces root respiration and nutrient content by converting living tissue to air volume. It was hypothesized that RCA increases soil resource acquisition by reducing the metabolic and phosphorus cost of soil exploration. To test the quantitative logic of the hypothesis, SimRoot, a functional-structural plant model with emphasis on root architecture and nutrient acquisition, was employed. Sensitivity analyses for the effects of RCA on the initial 40 d of growth of maize (Zea mays) and common bean (Phaseolus vulgaris) were conducted in soils with varying degrees of phosphorus availability. With reference to future climates, the benefit of having RCA in high CO(2) environments was simulated. The model shows that RCA may increase the growth of plants faced with suboptimal phosphorus availability up to 70 % for maize and 14 % for bean after 40 d of growth. Maximum increases were obtained at low phosphorus availability (3 µm). Remobilization of phosphorus from dying cells had a larger effect on plant growth than reduced root respiration. The benefit of both these functions was additive and increased over time. Larger benefits may be expected for mature plants. Sensitivity analysis for light-use efficiency showed that the benefit of having RCA is relatively stable, suggesting that elevated CO(2) in future climates will not significantly effect the benefits of having RCA. The results support the hypothesis that RCA is an adaptive trait for phosphorus acquisition by remobilizing phosphorus from the root cortex and reducing the metabolic costs of soil exploration. The benefit of having RCA in low-phosphorus soils is larger for maize than for bean, as maize is more sensitive to low phosphorus availability while it has a more 'expensive' root system. Genetic variation in RCA may be useful for breeding phosphorus-efficient crop cultivars, which is important for improving global food security.

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.

Rhizoeconomics: The Roots of Shoot Growth Limitations

The growth of terrestrial plants is primarily limited by edaphic factors such as drought, nutrient deficiencies, and mineral toxicities. Roots express an array of adaptive traits that help plants cope with these stresses, but such traits often incur significant costs, including direct metabolic costs, tradeoffs for contrasting resources, opportunity costs, and increased risks of biotic and abiotic stress. As an example, root cortical aerenchyma appears to improve crop growth under drought and low soil fertility by reducing the metabolic costs of soil exploration. Production of root cortical aerenchyma, however, may involve tradeoffs by reducing radial transport, mycorrhizal colonization, and by increasing disease susceptibility. A better understanding is needed of the full costs associated with specific root traits if we are to develop crops with better growth and yield in the stressful soil environments that increasingly dominate the earth's surface.