Phosphorus is an essential nutrient that is required for all major developmental processes and reproduction in plants. It is also a major constituent of the fertilizers required to sustain high-yield agriculture. Levels of phosphate--the only form of phosphorus that can be assimilated by plants--are suboptimal in most natural and agricultural ecosystems, and when phosphate is applied as fertilizer in soils, it is rapidly immobilized owing to fixation and microbial activity. Thus, cultivated plants use only approximately 20-30% of the applied phosphate, and the rest is lost, eventually causing water eutrophication. Recent advances in the understanding of mechanisms by which wild and cultivated species adapt to low-phosphate stress and the implementation of alternative bacterial pathways for phosphorus metabolism have started to allow the design of more effective breeding and genetic engineering strategies to produce highly phosphate-efficient crops, optimize fertilizer use, and reach agricultural sustainability with a lower environmental cost. In this review, we outline the current advances in research on the complex network of plant responses to low-phosphorus stress and discuss some strategies used to manipulate genes involved in phosphate uptake, remobilization, and metabolism to develop low-phosphate-tolerant crops, which could help in designing more efficient crops.

SUMMARYPhosphorus (P) is one of the essential nutrients for plants, and is indispensable for plant growth and development. P deficiency severely limits crop yield, and regular fertilizer applications are required to obtain high yields and to prevent soil degradation. To access P from the soil, plants have evolved high-and low-affinity Pi transporters and the ability to induce root architectural changes to forage P. Also, adjustments of numerous cellular processes are triggered by the P starvation response, a tightly regulated process in plants. With the increasing demand for food as a result of a growing population, the demand for P fertilizer is steadily increasing. Given the high costs of fertilizers and in light of the fact that phosphate rock, the source of P fertilizer, is a finite natural resource, there is a need to enhance P fertilizer use efficiency in agricultural systems and to develop plants with enhanced Pi uptake and internal P-use efficiency (PUE). In this review we will provide an overview of continuing relevant research and highlight different approaches towards developing crops with enhanced PUE. In this context, we will summarize our current understanding of root responses to low phosphorus conditions and will emphasize the importance of combining PUE with tolerance of other stresses, such as aluminum toxicity. Of the many genes associated with Pi deficiency, this review will focus on those that hold promise or are already at an advanced stage of testing (OsPSTOL1, AVP1, PHO1 and OsPHT1;6). Finally, an update is provided on the progress made exploring alternative technologies, such as phosphite fertilizer.

High crop yields depend on the continuous input of orthophosphate (PO(4)(−3))-based fertilizers and herbicides. Two major challenges for agriculture are that phosphorus is a nonrenewable resource and that weeds have developed broad herbicide resistance. One strategy to overcome both problems is to engineer plants to outcompete weeds and microorganisms for limiting resources, thereby reducing the requirement for both fertilizers and herbicides. Plants and most microorganisms are unable to metabolize phosphite (PO(3)(−3)), so we developed a dual fertilization and weed control system by generating transgenic plants that can use phosphite as a sole phosphorus source. Under greenhouse conditions, these transgenic plants require 30–50% less phosphorus input when fertilized with phosphite to achieve similar productivity to that obtained by the same plants using orthophosphate fertilizer and, when in competition with weeds, accumulate 2–10 times greater biomass than when fertilized with orthophosphate.

Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungusRhizophagus irregularisremarkably promoted rice (Oryza sativa) growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO3−supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter geneOsNPF4.5in rice roots, and its orthologsZmNPF4.5inZea maysandSbNPF4.5inSorghum bicolor. OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO3−transport activity when expressed inXenopus laevisoocytes. Moreover, knockout ofOsNPF4.5resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO3−was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO3−acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species.

SummaryMicroalgal cultivation that takes advantage of solar energy is one of the most cost‐effective systems for the biotechnological production of biofuels, and a range of high value products, including pharmaceuticals, fertilizers and feed. However, one of the main constraints for the cultivation of microalgae is the potential contamination with biological pollutants, such as bacteria, fungi, zooplankton or other undesirable microalgae. In closed bioreactors, the control of contamination requires the sterilization of the media, containers and all materials, which increases the cost of production, whereas open pond systems severely limits the number of species that can be cultivated under extreme environmental conditions to prevent contaminations. Here, we report the metabolic engineering of Chlamydomonas reinhardtii to use phosphite as its sole phosphorus source by expressing the ptxD gene from Pseudomonas stutzeri WM88, which encodes a phosphite oxidoreductase able to oxidize phosphite into phosphate using NAD as a cofactor. Engineered C. reinhardtii lines are capable of becoming the dominant species in a mixed culture when fertilized with phosphite as a sole phosphorus source. Our results represent a new platform for the production of microalgae, potentially useful for both closed photobioreactors and open pond systems without the need for using sterile conditions nor antibiotics or herbicides to prevent contamination with biological pollutants.

SignificanceAn increasing number of herbicide-resistant weeds are being reported in the United States, Argentina, and Brazil. This is becoming a global challenge for the production of several major crops, such as cotton, maize, and soybean. New strategies for weed control are required to sustain agricultural production while reducing our dependence on herbicides. Here, we report that selective fertilization of transgenic cotton, expressing a bacterial phosphite dehydrogenase (PTXD), with phosphite provides an effective way to suppress weed growth. Importantly, we show that the ptxD-transgenic cotton plants successfully outcompete a highly aggressive glyphosate-resistant weed. The ptxD/phosphite system represents one of the most promising technologies of recent times with potential to solve many of the agricultural and environmental problems that we encounter currently.

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Phosphorous (P) plays a critical role for all living organisms as a structural component of RNA, DNA and phospholipids. Microalgae are autotrophs organisms that have been reported to only assimilate the fully oxidized phosphate (Pi) as P source. However, there are microorganisms capable of utilizing P reduced compounds (i.e. phosphite (Phi) and hypophosphite) as a sole P source, such as bacteria and cyanobacteria. In this study, we evaluated whether microalgae, such as Chlamydomonas reinhardtii, Botryococcus braunii and Ettlia oleoabundans, are capable of using Phi as a sole P source. Our studies revealed that these three microalgae are unable to use Phi as a sole P source. We also found that when Phi is present at concentrations equal or higher than that of Pi, Phi has an inhibitory effect on C. reinhardtii growth. However, since C. reinhardtii was able to survive for a long period of cultivation in the presence of high concentrations of Phi and to recover cell division capacity after transfer to media containing Pi, we noticed that Phi is not toxic for this microalga. We propose that the inhibitory effect of Phi on C. reinhardtii growth might be caused, at least in part, by a competition between the transport of Pi and Phi.