Tailoring crop nutrition to fight weeds

Increasing crop productivity in an environmental-friendly way is one of the major challenges humankind is facing in the context of food security with a constantly growing population. In this scenario, ensuring adequate levels of soil nutrients and controlling aggressive weeds constitute two main problems that farmers have to deal with. Classical methods for weed control consist of onerous practices, such as hand weeding, or environmentally aggressive approaches like tilling cultivation. The discovery of the first herbicide, 2,4-dichlorophenoxyacetic acid, in 1940 (1) represented a breakthrough that greatly contributed to the improvement of weed control with a subsequent increase in crop yields. In addition, the application of herbicides led to a significant reduction of tillage operations, which had a direct beneficial consequence from the ecological point of view because of the decrease in CO₂ emissions associated with farming activities (2). Later on, the commercialization of Roundup, an herbicide based on glyphosate, in the 1970s provided an unprecedented powerful tool since Roundup was the first nonselective herbicide that eradicated most weeds germinating in soil. All these characteristics made Roundup the most successful and used herbicide in the history of agriculture. Nowadays, however, herbicides have become victims of their own success. Their massive employment has promoted the appearance of many herbicide-resistant weeds in crop fields. The existence of more than 254 herbicide-resistant weed species has been reported, of which 41 are glyphosate-resistant (3). This situation is boosting the necessity for constant research to find new molecules and strategies to control weed spreading. In PNAS, Pandeya et al. (4) report the development of an original and efficient strategy for weed control as an alternative to the utilization of classical herbicides. They demonstrate that selective fertilization of transgenic plants expressing a bacterial phosphite dehydrogenase (PTXD) with phosphite (Phi) provides an efficient way to restrain weed growth. The ptxD-transgenic plants are able to convert Phi into orthophosphate [Pi, the metabolizable form of phosphorus (P)], outcompeting different monocot and dicot weed species in both artificial substrates and natural soils from agricultural fields.

P is an essential nutrient for plant growth and development. Most plants absorb and assimilate P as inorganic Pi that, because of its chemical properties, is immobile, hampering its accessibility for plants (5). Furthermore, around 70% of arable lands have suboptimal availability of this ion, making soil amending with P fertilizers an essential practice to ensure high crop yields. The application of P fertilizers, however, has certain limitations that have to be considered. Soil microbiota competes with plants for this essential resource, converting P into insoluble inorganic forms or into unavailable organic forms. In fact, 80% of P fertilizers applied is lost by the action of these microorganisms (6). From an ecological point of view, since Pi is metabolizable by algae, excessive applications of P fertilizers promote the bloom of these organisms in aquatic ecosystems, causing eutrophication (7). More relevant, recent estimations indicate that the reserves of Pi in the earth are scarce and that, with the amounts that are being currently utilized, they will last only 50–200 y (8). Several laboratories have focused on developing plants with increased Pi use efficiency or new fertilization strategies. In 2012, López-Arredondo and Herrera-Estrella (9) proposed an original biotechnological approach to overcome the dependence of modern agriculture on Pi as a source of P. They overexpressed ptxD, a gene from Pseudomonas stutzeri encoding a Phi-specific oxidoreductase that oxidizes Phi to generate Pi, in Arabidopsis and tobacco. Data obtained clearly demonstrated that, under greenhouse conditions, ptxD-overexpressing plants were able to efficiently metabolize Phi into Pi. Interestingly, these plants required 30–50% less P when supplemented in the form of Phi instead of Pi to produce similar biomass (9). The application of Phi as a fertilizer provides several advantages. For instance, it has higher solubility and lower reactivity with soil components than Pi, and, additionally, soil microorganisms are unable to exploit it as a source of P. Furthermore, Phi is not metabolizable by algae; thus, it can be predicted that its implementation as a fertilizer will reduce the impact of Pi-based fertilizers in aquatic bodies. Plants, although able to absorb and mobilize Phi, cannot metabolize it either. Moreover, it has been shown that Phi negatively affects the growth of several plant species by interfering with Pi sensing systems (9). Based on this inhibitory activity, it was suggested that a potential additional advantage of the ptxD/Phi system could be its employment as a pre- and postemergence weed control agent (9, 10). Moreover, the inhibitory activity of Phi has also been used to develop a novel selectable system for transgenic plants of different species, including Arabidopsis, tobacco, cotton, and maize (11–14).

The study by Pandeya et al. (4) represents a relevant step toward validation of the ptxD/Phi system as a new strategy to overcome the problem caused by herbicide-resistant weeds in crop fields. As a first step, the authors demonstrate that transgenic cotton plants expressing the bacterial ptxD gene are able to utilize Phi as a source of P. Transgenic plants fertilized with Phi displayed similar biomass as wild-type plants supplemented with Pi, confirming the adequacy of changing the P source. Then, the authors performed various competition experiments with ptxD-transgenic cotton plants and different weeds to evaluate the efficiency of the ptxD/Phi system. In the first experiment, both a broadleaf weed and a grass weed were germinated together with transgenic cottons in a nonsterile inert substrate supplemented with Pi or Phi. The results indicated that Phi supplementation severely impaired the growth of both weed species, while transgenic cotton plants showed significantly increased biomass production compared with those supplemented with Pi. Similar results were obtained in competition experiments using natural soils from different locations that contained naturally occurring weed seeds. At this point, the main issue that remained to be determined was whether the ptxD/Phi system was also able to restrain the growth of a glyphosate-resistant weed, such as Amaranthus palmeri, which has well-known negative effects on the production of numerous crops (15). Data presented by Pandeya et al. (4) confirm that, in fact, Phi fertilization schemes severely inhibit the growth of A. palmeri when carried out on either inert artificial soil or nonsterile natural soil. The authors propose that the deleterious consequences of Phi on weed growth rely mainly on its capacity to inhibit P uptake. Additionally, they suggest that

The study by Pandeya et al. represents a relevant step toward validation of the ptxD/Phi system as a new strategy to overcome the problem caused by herbicide-resistant weeds in crop fields.

the competitive advantage of ptxD-transgenic plants allows them to outgrow the weeds, increasing the inhibitory effect of shading.

In summary, the results reported in the paper by Pandeya et al. (4) provide unbiased evidence demonstrating that the ptxD/Phi system constitutes a powerful control technology to suppress the growth of both broadleaf and grass weeds, including glyphosate-resistant species. These results, together with the already known benefits of substituting Phi by Pi as a fertilizer (discussed above), make the ptxD/Phi system a highly promising strategy not only to increase agricultural production but also to significantly reduce the impact of this activity on the environment (Fig. 1). As stressed by authors in their work, a highly remarkable asset of this technology is the low probability that Phi-resistant weeds could develop since that would imply the acquisition of completely new enzymatic activity to metabolize Phi, which would require several mutations in preexisting dehydrogenases. Moreover, in contrast to Pi, Phi can be obtained from different sources, such as from the recycling of waste products from industrial processes in which sodium hypophosphite is employed to reduce metal ions in chemical plating (i.e., nickel plating for decorative purposes) (5). Finally, it is worth mentioning that Phi does not represent any risk for human or animal health and is already being used extensively as an effective fungicide in agriculture (16). Nonetheless, taking into consideration the predicted expansive implementation of the ptxD/Phi technology in the near future, further studies are required to determine the potential and consequences that the application of Phi may have at different levels on the environment.

Fig. 1.

The ptxD/Phi system represents a very effective technology to suppress weed growth while providing adequate crop nutrition and reducing environmental problems. Pi-based fertilization allows weeds to compete with crops, such as cotton, for this P source, limiting their growth. In addition, a significant amount of Pi is metabolized by soil microorganisms, avoiding its accessibility to crops, or ends up in water bodies, promoting algae blooms and the subsequent eutrophication. When using the ptxD/Phi technology, the ability of transgenic crops to utilize Phi as a source of P and the inhibitory effect of Phi on weed development, including on herbicide-resistant weeds such as A. palmeri, boost crop growing. Furthermore, because of the low capability of soil microbiota to metabolize Phi, its availability for crops is highly increased. Similarly, algae cannot metabolize Phi either, decreasing the risk of eutrophication of water bodies.