Contents
I. Introduction  424
II. The phosphorus conundrum 424
III. Adaptations to low P 424
IV. Uptake of P  424
V. P deficiency alters root development and function 426
VI. P deficiency modifies carbon metabolism 431
VII. Acid phosphatase 436
VIII. Genetic regulation of P responsive genes 437
IX. Improving P acquisition 439
X. Synopsis  440


Summary
Phosphorus (P) is limiting for crop yield on > 30% of the world's arable land and, by some estimates, world resources of inexpensive P may be depleted by 2050. Improvement of P acquisition and use by plants is critical for economic, humanitarian and environmental reasons. Plants have evolved a diverse array of strategies to obtain adequate P under limiting conditions, including modifications to root architecture, carbon metabolism and membrane structure, exudation of low molecular weight organic acids, protons and enzymes, and enhanced expression of the numerous genes involved in low-P adaptation. These adaptations may be less pronounced in mycorrhizal-associated plants. The formation of cluster roots under P-stress by the nonmycorrhizal species white lupin (Lupinus albus), and the accompanying biochemical changes exemplify many of the plant adaptations that enhance P acquisition and use. Physiological, biochemical, and molecular studies of white lupin and other species response to P-deficiency have identified targets that may be useful for plant improvement. Genomic approaches involving identification of expressed sequence tags (ESTs) found under low-P stress may also yield target sites for plant improvement. Interdisciplinary studies uniting plant breeding, biochemistry, soil science, and genetics under the large umbrella of genomics are prerequisite for rapid progress in improving nutrient acquisition and use in plants.

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Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource

Phosphate (Pi) is considered to be one of the least available plant nutrients in the soil. High-affinity Pi transporters are generally accepted as entry points for Pi in the roots. The physiological, genetic, molecular and biochemical analysis of phosphate starvation response mechanisms highlight the ability of plants to adapt and thrive under phosphate limiting conditions. These responses help them enhance the availability of Pi, increase its uptake and improve the use-efficiency of Pi within a plant. Enhanced ability to acquire Pi appears to be regulated at the level of transcription of high-affinity phosphate transporters. These transporters are encoded by a family of small number of genes having characteristic tissue and organ associated expression patterns. Many of them are strongly induced during phosphate deficiency thus providing plants with enhanced ability to acquire and transfer phosphate. In addition, plants also activate biochemical mechanisms that could lead to increased acquisition of phosphate from both inorganic and organic phosphorus sources in the soil. Furthermore, altered root morphology and mycorrhizal symbiosis further enhance the ability of plants to acquire Pi. Interestingly most of these responses appear to be coordinated by changes in cellular phosphate levels. It is becoming apparent that phosphate acquisition and utilization are associated with activation or inactivation of a host of genes in plants. In this article we describe molecular, biochemical and physiological factors associated with phosphate acquisition by plants.

Phosphate Acquisition

Acid soils significantly limit crop production worldwide because approximately 50% of the world's potentially arable soils are acidic. Because acid soils are such an important constraint to agriculture, understanding the mechanisms and genes conferring tolerance to acid soil stress has been a focus of intense research interest over the past decade. The primary limitations on acid soils are toxic levels of aluminum (Al) and manganese (Mn), as well as suboptimal levels of phosphorous (P). This review examines our current understanding of the physiological, genetic, and molecular basis for crop Al tolerance, as well as reviews the emerging area of P efficiency, which involves the genetically based ability of some crop genotypes to tolerate P deficiency stress on acid soils. These are interesting times for this field because researchers are on the verge of identifying some of the genes that confer Al tolerance in crop plants; these discoveries will open up new avenues of molecular/physiological inquiry that should greatly advance our understanding of these tolerance mechanisms. Additionally, these breakthroughs will provide new molecular resources for improving crop Al tolerance via both molecular-assisted breeding and biotechnology.

How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency.

The rhizosphere is a complex environment where roots interact with physical, chemical and biological properties of soil. Structural and functional characteristics of roots contribute to rhizosphere processes and both have significant influence on the capacity of roots to acquire nutrients. Roots also interact extensively with soil microorganisms which further impact on plant nutrition either directly, by influencing nutrient availability and uptake, or indirectly through plant (root) growth promotion. In this paper, features of the rhizosphere that are important for nutrient acquisition from soil are reviewed, with specific emphasis on the characteristics of roots that influence the availability and uptake of phosphorus and nitrogen. The interaction of roots with soil microorganisms, in particular with mycorrhizal fungi and non-symbiotic plant growth promoting rhizobacteria, is also considered in relation to nutrient availability and through the mechanisms that are associated with plant growth promotion.

Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms

INTRODUCTION. Internal Organization of the Plant Body. Summary of Types of Cells and Tissues. General References. DEVELOPMENT OF THE SEED PLANT. The Embryo. From embryo to the Adult Plant. Apical Meristems and Their Derivatives. Differentiation, Specialization, and Morphogenesis. References. THE CELL. Cytoplasm. Nucleus. Plastids. Mitochondria. Microbodies. Vacuoles. Paramural Bodies. Ribosomes. Dictyosomes. Endoplasmic Reticulum. Lipid Globules. Microtubules. Ergastic Substances. References. CELL WALL. Macromolecular Components and Their Organization in the Wall. Cell Wall Layers. Intercellular Spaces. Pits, Primary Pit--Fields, and Plasmodesmata. Origin of Cell Wall During Cell Division. Growth of Cell Wall. References. PARENCHYMA AND COLLENCHYMA. Parenchyma. Collenchyma. References. SCLERENCHYMA. Sclereids. Fibers. Development of Sclereids and Fibers. References. EPIDERMIS. Composition. Developmental Aspects. Cell Wall. Stomata. Trichomes. References. XYLEM: GENERAL STRUCTURE AND CELL TYPES. Gross Structure of Secondary Xylem. Cell Types in the Secondary Xylem. Primary Xylem. Differentiation of Tracheary Elements. References. XYLEM: VARIATION IN WOOD STRUCTURE. Conifer Wood. Dicotyledon Wood. Some Factors in Development of Secondary Xylem. Identification of Wood. References. VASCULAR CAMBIUM. Organization of Cambium. Developmental Changes in the Initial Layer. Patterns and Causal Relations in Cambial Activity. References. PHLOEM. Cell Types. Primary Phloem. Secondary Phloem. References. PERIDERM. Structure of Periderm and Related Tissues. Development of Periderm. Outer Aspect of Bark in Relation to Structure. Lenticels. References. SECRETORY STRUCTURES. External Secretory Structures. Internal Secretory Structures. References. THE ROOT: PRIMARY STATE OF GROWTH. Types of Roots. Primary Structure. Development. References. THE ROOT: SECONDARY STATE OF GROWTH AND ADVENTITIOUS ROOTS. Common Types of Secondary Growth. Variations in Secondary Growths. Physiologic Aspects of Secondary Growth in Roots. Adventitious Roots. References. THE STEM: PRIMARY STATE OF GROWTH. External Morphology. Primary Structure. Development. References. THE STEM: SECONDARY GROWTH AND STRUCTURAL TYPES. Secondary Growth. Types of Stems. References. THE LEAF: BASIC STRUCTURE AND DEVELOPMENT. Morphology. Histology of Angiosperm Leaf. Development. Abscission. References. THE LEAF: VARIATIONS IN STRUCTURE. Leaf Structure and Environment. Dicotyledon Leaves. Monocotyledon Leaves. Gymnosperm Leaves. References. THE FLOWER: STRUCTURE AND DEVELOPMENT. Concept. Structure. Development. References. THE FLOWER: REPRODUCTIVE CYCLE. Microsporogenesis. Pollen. Male Gametophyte. Megasporogenesis. Female Gametophyte. Fertilization. References. THE FRUIT. Concept and Classification. The Fruit Wall. Fruit Types. Fruit Growths. Fruit Abscission. References. THE SEED. Concept and Morphology. Seed Development. Seed Coat. Nutrient Storage Tissues. References. EMBRYO AND SEEDLING. Mature Embryo. Development of Embryo. Classification of Embryos. Seedling. References. Glossary. Index.

Anatomy of Seed Plants

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.

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

We present a method to visually score 10 root architectural traits of the root crown of an adult maize plant in the field in a few minutes. Phenotypic profiling of three recombinant inbred line (RIL) populations of maize (Zea mays L.; B73xMo17, Oh43xW64a, Ny821xH99) was conducted in 2008 in a silt loam soil in Pennsylvania and in a sandy soil in Wisconsin, and again in 2009 in Pennsylvania. Numbers, angles and branching pattern of crown and brace roots were assessed visually at flowering. Depending on the soil type in which plants were grown, sample processing took from three (sand) to 8 min (silt-loam). Visual measurement of the root crown required 2 min per sample irrespective of the environment. Visual scoring of root crowns gave a reliable estimation of values for root architectural traits as indicated by high correlations between measured and visually scored trait values for numbers (r2 = 0.46–0.97), angles (r2 = 0.66–0.76), and branching (r2 = 0.54–0.88) of brace and crown roots. Based on the visual evaluation of root crown traits it was possible to discriminate between populations. RILs derived from the cross NY821 x H99 generally had the greatest number of roots, the highest branching density and the most shallow root angles, while inbred lines from the cross between OH43 x W64a generally had the steepest root angles. The ranking of genotypes remained the same across environments, emphasizing the suitability of the method to evaluate genotypes across environments. Scoring of brace roots was better correlated with the actual measurements compared to crown roots. The visual evaluation of root architecture will be a valuable tool in tailoring crop root systems to specific environments.

Shovelomics: high throughput phenotyping of maize ( Zea mays L.) root architecture in the field

Root architectural traits that increase topsoil foraging are advantageous for phosphorus acquisition but may incur tradeoffs for the acquisition of deep soil resources such as water. To examine this relationship, common bean genotypes contrasting for rooting depth were grown in the field and in the greenhouse with phosphorus stress, water stress and combined phosphorus and water stress. In the greenhouse, water and phosphorus availability were vertically stratified to approximate field conditions, with higher phosphorus in the upper layer and more moisture in the bottom layer. Under phosphorus stress, shallow-rooted genotypes grew best, whereas under drought stress, deep-rooted genotypes grew best. In the combined stress treatment, the best genotype in the greenhouse had a dimorphic root system that permitted vigorous rooting throughout the soil profile. In the field, shallow-rooted genotypes surpassed deep-rooted genotypes under combined stress. This may reflect the importance of early vegetative growth in terminal drought environments. Our results support the hypothesis that root architectural tradeoffs exist for multiple resource acquisition, particularly when resources are differentially localised in the soil profile. Architectural plasticity and root dimorphism achieved through complementary growth of distinct root classes may be important means to optimise acquisition of multiple soil resources.

/pdf/root-architectural-tradeoffs-for-water-and-phosphorus-4927l89tf5.pdf

Root architectural tradeoffs for water and phosphorus acquisition

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 aminooxyacetic 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.

https://www.onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-3040.2001.00695.x

Regulation of root hair density by phosphorus availability in Arabidopsis thaliana

A substantial body of literature supports the involvement of ethylene in abscission of leaves, flowers and flower parts, and fruit. Exogenous ethylene accelerates abscission in many, but not all, abscising plant systems. In some cases, endogenous ethylene production increases before abscission, while in others a change in ethylene sensitivity can be demonstrated. Ethylene interacts with auxin in regulating abscission, particularly in leaves and fruit. Ethylene has been shown to regulate expression of genes involved in cell separation, including cellulases and pectinases. Such regulation has been demonstrated at the level of mRNA abundance, but post-transcriptional regulation may also be important.

Kathleen M. Brown

Papers

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

Shovelomics: high throughput phenotyping of maize ( Zea mays L.) root architecture in the field

Root architectural tradeoffs for water and phosphorus acquisition

Regulation of root hair density by phosphorus availability in Arabidopsis thaliana

Ethylene and abscission