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.
Low phosphorus availability induces the formation of cortical aerenchyma in roots. The adaptive significance of this response is unknown. We hypothesized that aerenchyma may be helpful to low-phosphorus plants by reducing root respiratory and phosphorus requirements, thereby increasing the metabolic efficiency of soil exploration. To test this hypothesis we investigated aerenchyma formation, root respiration and tissue phosphorus concentration in maize and common bean genotypes in response to phosphorus availability and ethylene treatments. Genotypes differed substantially in their ability to form aerenchyma in response to low phosphorus. Aerenchyma formation was disproportionately correlated with reduced root respiration; roots with 30% cross-sectional area as aerenchyma had 70% less respiration than roots without aerenchyma. Aerenchyma formation was also proportionally correlated with reduced root phosphorus concentration. Variation in aerenchyma formation was correlated with root respiration and phosphorus concentration, regardless of whether such variation was caused genetically or by ethylene or phosphorus treatments. Results with isolated roots were confirmed by measurement of whole root respiration of intact maize plants. Our results support the hypothesis that aerenchyma formation reduces the respiratory and phosphorus requirements of soil exploration by roots, and thus, represents a useful adaptation to low phosphorus availability.
Previous work on the adaptation of maize (Zea mays) primary roots to water deficit showed that cell elongation is maintained preferentially toward the apex, and that this response involves modification of cell wall extension properties. To gain a comprehensive understanding of how cell wall protein (CWP) composition changes in association with the differential growth responses to water deficit in different regions of the elongation zone, a proteomics approach was used to examine water soluble and loosely ionically bound CWPs. The results revealed major and predominantly region-specific changes in protein profiles between well-watered and water-stressed roots. In total, 152 water deficit-responsive proteins were identified and categorized into five groups based on their potential function in the cell wall: reactive oxygen species (ROS) metabolism, defense and detoxification, hydrolases, carbohydrate metabolism, and other/unknown. The results indicate that stress-induced changes in CWPs involve multiple processes that are likely to regulate the response of cell elongation. In particular, the changes in protein abundance related to ROS metabolism predicted an increase in apoplastic ROS production in the apical region of the elongation zone of water-stressed roots. This was verified by quantification of hydrogen peroxide content in extracted apoplastic fluid and by in situ imaging of apoplastic ROS levels. This response could contribute directly to the enhancement of wall loosening in this region. This large-scale proteomic analysis provides novel insights into the complexity of mechanisms that regulate root growth under water deficit conditions and highlights the spatial differences in CWP composition in the root elongation zone.Roots often continue to grow under water deficits that completely inhibit shoot and leaf elongation (Sharp and Davies, 1979;Westgate and Boyer, 1985), and this is considered an important mechanism of plant adaptation to water-limited conditions (Sharp and Davies, 1989). Investigation of the mechanisms of root growth adaptation to water deficit is important for improving plant performance under drought, because water resources for agriculture are becoming increasingly limited.The physiology of maize (Zea mays) primary root elongation at low water potentials has been studied extensively (for review, see Sharp et al., 2004), which has provided the foundation for an understanding of the complex network of responses involved. Analysis of the relative elongation rate profile within the root elongation zone showed that under severe water deficit, elongation rates are fully maintained in the apical few millimeters but progressively inhibited as cells are displaced further from the root apex (Sharp et al., 1988;Liang et al., 1997). To help understand the maintenance of elongation in the apical region of roots growing under water deficit conditions, Spollen and Sharp (1991) measured the spatial distribution of turgor pressure and found that values were uniformly decreased by over 50% throughout the e...
Low soil phosphorus availability is a primary constraint for plant growth in many terrestrial ecosystems. Lateral root initiation and elongation may play an important role in the uptake of immobile nutrients, such as phosphorus, by increasing soil exploration and phosphorus solubilisation. The overall objective of this study was to assess the value of lateral rooting for phosphorus acquisition through assessment of the 'benefit' of lateral rooting for phosphorus uptake and the 'cost' of lateral roots in terms of root respiration and phosphorus investment at low and high phosphorus availability. Five recombinant inbred lines (RILs) of maize derived from a cross between B73 and Mo17 with contrasting lateral rooting were grown in sand culture in a controlled environment. Genotypes with enhanced or sustained lateral rooting at low phosphorus availability had greater phosphorus acquisition, biomass accumulation, and relative growth rate (RGR) than genotypes with reduced lateral rooting at low phosphorus availability. The association of lateral root development and plant biomass accumulation under phosphorus stress was not caused by allometry. Genotypes varied in the phosphorus investment required for lateral root elongation, owing to genetic differences in specific root length (SRL, which was correlated with root diameter) and phosphorus concentration of lateral roots. Lateral root extension required less biomass and phosphorus investment than the extension of other root types. Relative growth rate was negatively correlated with specific root respiration, supporting the hypothesis that root carbon costs are an important aspect of adaptation to low phosphorus availability. Two distinct cost-benefit analyses, one with phosphorus acquisition rate as a benefit and root respiration as a cost, the other with plant phosphorus accumulation as a benefit and phosphorus allocation to lateral roots as a cost, both showed that lateral rooting was advantageous under conditions of low phosphorus availability. Our data suggest that enhanced lateral rooting under phosphorus stress may be harnessed as a useful trait for the selection and breeding of more phosphorus-efficient maize genotypes.
Low phosphorus availability is a primary constraint for plant growth in terrestrial ecosystems. Lateral root initiation and elongation may play an important role in the uptake of immobile nutrients such as phosphorus by increasing soil exploration and phosphorus acquisition. The objective of this study was to identify quantitative trait loci (QTLs) controlling lateral root length (LRL), number (LRN), and plasticity of the primary seedling root of maize under varying phosphorus availability. Using a cigar roll culture in a controlled environment, we evaluated primary root LRL and LRN at low and high phosphorus availability in 160 recombinant inbred lines (RILs) derived from a cross between maize genotypes B73 and Mo17, which have contrasting adaptation to low phosphorus availability in the field. Low phosphorus availability increased LRL by 19% in Mo17, the phosphorus-efficient parent, but significantly decreased LRL in B73, the phosphorus-inefficient genotype. Substantial genetic variation and transgressive segregation for LRL and LRN existed in the population. The plasticity of LRL ranged from -100% to 146.3%, with a mean of 30.4%, and the plasticity of LRN ranged from -82.2% to 164.1%, with a mean of 18.5%. On the basis of composite interval mapping with a LOD threshold of 3.27, one QTL was associated with LRN plasticity, five QTLs were associated with LRL and one QTL was associated with LRN under high fertility. Under low fertility, six QTLs were associated with LRL and one QTL with LRN. No QTLs were detected for plasticity of LRL. A number of RILs exceeded Mo17, the phosphorus-efficient parent, for LRL, LRN, and plasticity. The detection of QTLs for these traits, in combination with the observation of transgressive segregants in our population, indicates that favorable alleles can be combined to increase seedling lateral root growth in maize.
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.
In soybean and common bean, enhanced topsoil foraging permitted by shallow root architectures is advantageous for phosphorus acquisition from stratified soils. The importance of this phenomenon in graminaceous crops, which have different root architecture and morphology from legumes, is unclear. In this study we evaluated the importance of shallow roots for phosphorus acquisition in maize (Zea mays L.). In a field study, maize genotypes with shallower roots had greater growth in low phosphorus soil than deep-rooted genotypes. For physiological analysis, four maize genotypes differing in root shallowness in the field were grown in solid media with stratified phosphorus availability in a controlled environment. Of the four genotypes, one shallow and one deep genotype were also inoculated with arbuscular mycorrhiza (AM). Shallower genotypes had significantly greater growth and phosphorus accumulation compared with deeper genotypes at low phosphorus availability. Mycorrhizal colonisation altered root shallowness under low phosphorus conditions, increasing shallowness substantially in a deep-rooted genotype but slightly decreasing shallowness in a shallow-rooted genotype. Mycorrhizal colonisation increased phosphorus acquisition under low phosphorus availability. Respiration costs of roots and shoots of phosphorusefficient genotypes were significantly lower under low phosphorus conditions compared with inefficient genotypes. The physiological efficiency of phosphorus acquisition, expressed as root respiration per unit of phosphorus acquisition, was greater in shallow rooted genotypes. Our results demonstrate that genetic variation for root shallowness exists in maize, that phosphorus and AM can modulate root shallowness independently, and that a shallower root system is beneficial for plant performance in maize at low phosphorus availability. We propose that root architectural traits that enhance topsoil foraging are important traits for improved phosphorus acquisition efficiency of annual grain crops such as maize in addition to legumes.
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