Plant and microbial strategies to improve the phosphorus efficiency of agriculture

Background

Agricultural production is often limited by low phosphorus (P) availability. In developing countries, which have limited access to P fertiliser, there is a need to develop plants that are more efficient at low soil P. In fertilised and intensive systems, P-efficient plants are required to minimise inefficient use of P-inputs and to reduce potential for loss of P to the environment.

Scope

Three strategies by which plants and microorganisms may improve P-use efficiency are outlined: (i) Root-foraging strategies that improve P acquisition by lowering the critical P requirement of plant growth and allowing agriculture to operate at lower levels of soil P; (ii) P-mining strategies to enhance the desorption, solubilisation or mineralisation of P from sparingly-available sources in soil using root exudates (organic anions, phosphatases), and (iii) improving internal P-utilisation efficiency through the use of plants that yield more per unit of P uptake.

Conclusions

We critically review evidence that more P-efficient plants can be developed by modifying root growth and architecture, through manipulation of root exudates or by managing plant-microbial associations such as arbuscular mycorrhizal fungi and microbial inoculants. Opportunities to develop P-efficient plants through breeding or genetic modification are described and issues that may limit success including potential trade-offs and trait interactions are discussed. Whilst demonstrable progress has been made by selecting plants for root morphological traits, the potential for manipulating root physiological traits or selecting plants for low internal P concentration has yet to be realised.     

Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation

Plants require the function of plasma membrane-bound sulphate transporters for the initial uptake of inorganic sulphate. Part of this fundamental process is the energy-dependent proton/sulphate co-transport systems that are located in the surface cell layers of roots. During sulphur limitation, plants are able to activate the expression of sulphate transporters that facilitate the uptake of sulphate in roots. SULTR1;1 and SULTR1;2 are suggested to be the essential components of the sulphate uptake system in Arabidopsis roots. The physiological importance of SULTR1;1 and SULTR1;2 is supported by characteristics that can cope with sulphur deficiency: they were (i) functional high-affinity sulphate transporters; (ii) induced by sulphur limitation at the mRNA levels; and (iii) predominantly localized in the root hairs, epidermis, and cortex. The expression of high-affinity sulphate transporters was primarily regulated by sulphur in a promoter-dependent manner. Aside from the sulphur-specific regulation, the induction of SULTR1;1 and SULTR1;2 high-affinity sulphate transporters by sulphur limitation was dependent on the supply of carbon and nitrogen. In this review, the application of SULTR promoter-GFP systems for the analysis of regulatory pathways of sulphate acquisition in plants is described.     

Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport

Proton/sulphate co-transport in the plasma membrane of root cells is the first step for the uptake of sulphate from the environment by plants. Further intracellular, cell-to-cell and long-distance transport must fulfil the requirements for sulphate assimilation and source/sink demands within the plant. A gene family of sulphate transporters, which may be subdivided into five groups, has been identified with examples from many different plant species. For at least two groups, proton/sulphate co-transport activity has been confirmed. It appears that each group represents sulphate transporters with distinct kinetic properties, patterns of expression, and cell/tissue specificity related to specific roles in the uptake and allocation of sulphate. High-affinity sulphate uptake and low-affinity vascular transport, as well as vacuolar efflux, are controlled by the nutritional status of the plant. Most notably there is an apparent increase in capacity for cellular sulphate uptake and vacuolar efflux when sulphur supply is limiting. Within the groups, the individual sulphate transporters may be further subdivided by differences in temporal, cellular and tissue expression. Many of the transporters are regulated by the nutritional status of the individual tissues, to optimize sulphate movement within and between sink and source organs.     

Responses of two wheat varieties to sulphur addition and diagnosis of sulphur deficiency

Sulphur deficiency has become increasingly widespread in wheat in the U.K. Growth, nutrient content and biochemical responses to S and N supply of a breadmaking wheat variety (Hereward) and a non-breadmaking variety (Riband) were investigated in a pot experiment. Shoot dry matter (DM) at stem extension (Zadok's GS 37) and at maturity was increased markedly by S. Grain production of the Riband variety was more susceptible to the imbalance of N to S than the Hereward variety. At GS 37, the concentrations of total S and sulphate-S of shoots, chlorophyll meter readings and the concentrations of glutathione of the uppermost fully expanded leaves were increased significantly by increasing S supply, whereas the concentrations of nitrate and amides were decreased by S. The greatest relative changes in response to S supply were those of the glutathione and asparagine concentrations. Riband also showed greater response to S than Hereward. Critical values of various diagnostic indices at GS 37 were derived from the relationships between DM yield and different indices. The two varieties showed similar diagnostic curves except that for the ratio of total N to total S (N:S) in shoots. Either total S or sulphate-S can be used alone as a good indicator of deficiency, and with values of 1500 and 190 mg kg^-1 DM in shoots for the two indices respectively. There was also a well defined relationship between DM yield and the glutathione concentration, with a critical value of 240 nmol g^-1 FW. There were no advantages of using % of total S as sulphate-S. Shoot N:S ratio was found to be less accurate in predicting S deficiency than total S or sulphate-S. For prognostic purposes, a much higher S status at GS 37 was required to ensure no losses of DM yield due to S deficiency at maturity.     

Tools for high efficiency genetic manipulation of the human pathogen Penicillium marneffei

Penicillium marneffei is an opportunistic pathogen of humans and displays a temperature dependent dimorphic transition. Like many fungi, exogenous DNA introduced by DNA mediated transformation is integrated randomly into the genome resulting in inefficient gene deletion and position-specific effects. To enhance successful gene targeting, the consequences of perturbing components of the non-homologous end joining recombination pathway have been examined. The deletion of the KU70 and LIG4 orthologs, pkuA and ligD, respectively, dramatically enhanced the observed homologous recombination frequency leading to efficient gene deletion. While ΔpkuA was associated with reduced genetic stability over-time, ΔligD represents a suitable recipient strain for downstream applications and combined with a modified Gateway? system for the rapid generation of gene deletion constructs, this represents an efficient pipeline for characterizing gene function in P. marneffei.     

Extractable sulphate and organic sulphur in soils and their availability to plants

Ten soils collected from the major arable areas in Britain were used to assess the availability of soil sulphur (S) to spring wheat in a pot experiment. Soils were extracted with various reagents and the extractable inorganic SO₄-S and total soluble S(SO₄-S plus a fraction of organic S) were determined using ion chromatography (IC) or inductively-coupled plasma atomic emission spectrometry (ICP-AES), respectively. Water, 0.016 M KH₂PO₄, 0.01 M CaCl₂ and 0.01 M Ca(H₂PO₄)₂ extracted similar amounts of SO₄-S, as measured by IC, which were consistently smaller than the total extractable S as measured by ICP-AES. The amounts of organic S extracted varied widely between different extractants, with 0.5 M NaHCO₃ (pH 8.5) giving the largest amounts and 0.01 M CaCl₂ the least. Organic S accounted for approximately 30–60% of total S extracted with 0.016 M KH₂PO₄ and the organic C:S ratios in this extract varied typically between 50 and 70. The concentrations of this S fraction decreased in all soils without added S after two months growth of spring wheat, indicating a release of organic S through mineralisation. All methods tested except 0.5 M NaHCO₃-ICP-AES produced satisfactory results in the regression with plant dry matter response and S uptake in the pot experiment. In general, 0.016 M KH₂PO₄ appeared to be the best extractant and this extraction followed by ICP-AES determination was considered to be a good method to standardise on.     

Plant uptake of sulphur as related to changes in the HI-reducible and total sulphur fractions in soil

Although considerable progress has been made in relating extractable soil S to plant S availability, most of these studies determined the extractable soil S at the beginning of the experiment to use as an index of soil S status. This bears little or no relationship to the S taken up by plants during the entire growing season. The present study investigates the changes in extractable soil S with time and relates these to changes in plant S uptake. Six soils with different long-term fertiliser histories (0, 21, 42 kg of S as superphosphate ha^–1 applied since 1952) and animal camping treatments (camp and non-camp) were used in two pot systems (with and without plants). Carrier-free ³⁵SO₄–S was added to the soils, to provide the information on the transformations of recently added S between the different extractable S forms in soils and whether these transformations could predict plant-available S. The soils were pre-conditioned and then transferred to the glasshouse, where one set of pots were planted with perennial ryegrass (Lolium perenne L.) while the other set was left uncropped. Periodic plant harvests and soil samplings at four weekly intervals were conducted over a period of 20 weeks to determine plant S uptake and amounts of extractable soil S and ³⁵S forms using five extractants. Same extractions of soil S and ³⁵S were conducted for the initial soils. Results showed that HI-reducible and total soil S extracted by CaCl₂, KH₂PO₄ and by KCl at 40°C were utilised significantly by plants but not those extracted by NaHCO₃ and NaOH extractants. However, after the 8th week, plants continued to take up S even though levels of S extracted from the soil by CaCl₂, KH₂PO₄ and by KCl at 40°C remained low and unchanged. These results suggest that soil S taken up by plants after the 8th week period originated directly from the mineralisation of soil organic S from S pools other than those present in the extractable soil S forms. Similar results were shown by ³⁵S data, thereby confirming the complexity of determining plant S availability based on soil S extraction methods.     

Gene chip analyses reveal differential genetic responses to iron deficiency in rat duodenum and jejunum

Previous studies revealed novel genetic changes in the duodenal mucosa of iron-deprived rats during postnatal development. These observations are now extended to compare the genetic response to iron deficiency in the duodenum versus jejunum of 12-wk-old rats. cRNA samples were prepared from the duodenal and jejunal mucosa of three groups each of control and iron-deficient rats and hybridized with RAE 230A and 230B gene chips (Affymetrix). Stringent data reduction strategies were employed. Results showed that several genes were similarly induced in both gut segments, including DMT1, Dcytb, transferrin receptor 1, heme oxygenase 1, metallothionein, the Menkes copper ATPase (ATP7A), tripartitie motif protein 27, and the sodium-dependent vitamin C transporter. However, a subset of genes showed regulation in only one or the other gut segment. In duodenum only, gastrokine 1, trefoil factor 1 and claudin 2 were induced by iron-deficiency. Other genes previously identified were only regulated in the duodenum. Overall, these studies demonstrate similarities and distinct differences in the genetic response to iron deprivation in the duodenum versus jejunum and provide evidence that more distal gut segments also may play a role in increasing iron absorption in iron-deficiency anemia.     

The manipulation of zein genes to improve the nutritional value of corn

The zein genes from corn (maize) were among the first plant genes to be isolated by recombinant DNA techniques. They encode a set of proteins which are of agricultural importance. Over 2 billion bushels of corn are fed to poultry and pigs each year in the USA alone. However the nutritional balance of corn is not ideal and thus farmers must buy expensive feed supplements. By changing the composition of zein proteins, genetic engineers might produce savings of many million dollars a year.     

Differential responses of freshwater wetland soils to sulphate pollution

Sulphate (SO₄ ^2-)reduction rates are generally low in freshwaterwetlands and are regulated by the scarceavailability of the ion. Increasedconcentrations of this electron acceptor due tosulphur (S) pollution of groundwater andsurface water may, however, lead to highSO₄ ^2- reduction rates now regulatedby the availability of appropriate electrondonors. Due to variations in this availability,the response to S pollution (e.g. from surfacewater or groundwater) is expected to differbetween soils. This hypothesis was tested inlaboratory mesocosm experiments by comparingtwo wetland soil types with distinctlydifferent humus profiles: a Hydromoder and aRhizomull type. In the first type, expected tohave a higher availability of degradable soilorganic matter (SOM), SO₄ ^2-availability appeared to be rate limiting forSO₄ ^2- reduction. In the Rhizomullsoils, in contrast, the electron acceptor didnot limit SO₄ ^2- reduction rates athigher concentrations. These differences inresponse could not, however, be attributed todifferences in the various SOM fractions or inSOM densities. Eutrophication and free sulphideaccumulation, two major biogeochemical problemscaused by SO₄ ^2- pollution, occurredin both types. The absolute extent ofphosphorus mobilisation was determined by theconcentration of this element in the soil (C/Pratio), while the level of sulphideaccumulation was governed by the concentrationof dissolved iron in the pore water. It wastherefore concluded that neither the humusprofile nor the concentrations of different SOMfractions in the soils are reliable indicatorsfor the sensitivity of wetland types to Spollution.     

Plant responses to drought and rewatering

Plants would be more vulnerable to water stress and thereafter rewatering or a cycled water environmental change, which occur more frequently under climatic change conditions in terms of the prediction scenarios. Effects of water stress on plants alone have been well-documented in many reports. However, the combined responses to drought and rewatering and its mechanism are relatively scant. As we know, plant growth, photosynthesis and stomatal aperture may be limited under water deficit, which would be regulated by physical and chemical signals. Under severe drought, while peroxidation may be provoked, the relevant antioxidant metabolism would be involved to annihilate the damage of reactive oxygen species. As rewatering, the recoveries of plant growth and photosynthesis would appear immediately through growing new plant parts, re-opening the stomata, and decreasing peroxidation; the recovery extents (reversely: pre-drought limitation) due to rewatering strongly depend on pre-drought intensity, duration and species. Understanding how plants respond to episodic drought and watering pulse and the underlying mechanism is remarkably helpful to implement vegetation management practices in climatic changing.Key words: drought stress, peroxidation, photosynthesis, relative growth rate, pre-drought limitation, rewatering, signals, stomatal conductanceUnder the climatic changing context, drought has been, and is becoming an acute problem most constraining plant growth, terrestrial ecosystem productivity, in many regions all over the world, particularly in arid and semi-arid area.^1–3 Based on the fourth assessment report by IPCC, global surface average temperature will have a 1.1–6.4°C range increase by the end of this century.³ It is indicated that a warming above 3°C would eliminate thoroughly fixed carbon function of global terrestrial vegetation, shift a net carbon source. With global warming, it is expected that water deficit would be escalated by increasing evapotranspiration, increasing the frequency and intensity of drought with an increase from 1% to 30% in extreme drought land area by 2100;³ which would offset the beneficial effect from the elevated CO₂ concentration, further limiting the structure and function of the terrestrial ecosystem. The global climate models may forecast the precipitation regimes including its distribution and amount, but the complicated responses of terrestrial ecosystem to climate change may adversely affect the predict accuracy.^1,4Plant would response to water stress by dramatically complex mechanisms from genetic molecular express, biochemical metabolism through individual plant physiological processes to ecosystem levels^2,5,6 which may mainly includes six aspects: (1) drought escape via completing plant life cycle before severe water deficit. E.g., earlier flowering in annuals species before the onset of severe drough;⁷ (2) drought avoidance via enhancing capacity of getting water. E.g., developing root systems or conserving it such as reduction of stomata and leaf area/canopy cover;^8,9 (3) drought tolerance mainly via improving osmotic adjustment ability and increasing cell wall elasticity to maintain tissue turgidity;¹⁰ (4) drought resistance via altering metabolic path for life survives under severe stress (e.g., increased antioxidant metabolism);^11,12 (5) drought abandon by removing a part of individual, e.g., shedding elder leaves under water stress;² (6) drought-prone biochemical-physiological traits for plant evolution under long-term drought condition via genetic mutation and genetic modification.^13–15 The processes may be involved in multi-aspects simultaneously in responses of plants to drought stress and thereafter rewatering.In the field context, there is always interval occurrence in drought and/or rewetting events, particular under climatic change conditions predicting more frequent drought and flooding events.³ The water cycle change may greatly impact plant growth, photosynthesis and many key metabolic functions, thereby ecosystem productivity and agricultural achievement.^5,16–18 Actually, sporadic precipitation would become a critical issue for maintaining ecosystem structural stability and even it''s surviving in arid and semi-arid area. For example, a small rainfall pulse can induce a rapid response in a desert ecosystem, which quickly triggers plant growth so that the plants can survive.¹⁹ Thus, to highlight how plant and terrestrial ecosystem cope with adverse abnormal climatic change variables is, and always will be crucial research issue in practical management of plant growth and vegetation productivity. Here, we try to provide a brief insight into how plant responses to the pre-drought and rewatering in terms of the plant growth, gas exchange and key related-physiological processes such as reactive oxygen species (ROS) metabolism. Finally a regulation path schematic is presented to try to explain the involved processes.