Plant secondary metabolite-dependent plant-soil feedbacks can improve crop yield in the field
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eLife assessment
This study presents findings that are important for understanding plant-soil feedbacks in agriculture. The authors use a large-scale agricultural field experiment to demonstrate the role of root-emitted secondary metabolites in enhancing the yield of the next crop. By using a benzoxazinoid-deficient maize genotype, the authors provide compelling evidence that biomass production and grain yield of several wheat varieties can be increased when grown in soil conditioned by maize plants able to release benzoxazinoids.
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Abstract
Plant secondary metabolites that are released into the rhizosphere alter biotic and abiotic soil properties, which in turn affect the performance of other plants. How this type of plant-soil feedback affects agricultural productivity and food quality in the field in the context of crop rotations is unknown. Here, we assessed the performance, yield and food quality of three winter wheat varieties growing in field plots whose soils had been conditioned by either wild type or benzoxazinoid-deficient bx1 maize mutant plants. Following maize cultivation, we detected benzoxazinoid-dependent chemical and microbial fingerprints in the soil. The benzoxazinoid fingerprint was still visible during wheat growth, but the microbial fingerprint was no longer detected. Wheat emergence, tillering, growth, and biomass increased in wild type conditioned soils compared to bx1 mutant conditioned soils. Weed cover was similar between soil conditioning treatments, but insect herbivore abundance decreased in benzoxazinoid-conditioned soils. Wheat yield was increased by over 4% without a reduction in grain quality in benzoxazinoid-conditioned soils. This improvement was directly associated with increased germination and tillering. Taken together, our experiments provide evidence that soil conditioning by plant secondary metabolite producing plants can increase yield via plant-soil feedbacks under agronomically realistic conditions. If this phenomenon holds true across different soils and environments, optimizing root exudation chemistry could be a powerful, genetically tractable strategy to enhance crop yields without additional inputs.
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eLife assessment
This study presents findings that are important for understanding plant-soil feedbacks in agriculture. The authors use a large-scale agricultural field experiment to demonstrate the role of root-emitted secondary metabolites in enhancing the yield of the next crop. By using a benzoxazinoid-deficient maize genotype, the authors provide compelling evidence that biomass production and grain yield of several wheat varieties can be increased when grown in soil conditioned by maize plants able to release benzoxazinoids.
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Reviewer #1 (Public Review):
This is a very interesting and timely manuscript investigating the roles of root-emitted secondary metabolites in mediating plant-soil feedback in a realistic and agricultural context (maize - wheat rotation). I find this article to be an important contribution to the field as the roles played by soil chemical legacies in mediating plant-soil feedbacks have been largely overlooked so far, particularly in the field. I found this manuscript to be extremely well-written and clear. I was impressed by the number of response variables measured by the authors to characterise how wheat plants responded to the soil legacies created by different maize genotypes.
The article presents the results of a plant-soil feedback experiment in which two maize genotypes (wild type or benzoxazinoid-deficient bx1 mutant plant) …Reviewer #1 (Public Review):
This is a very interesting and timely manuscript investigating the roles of root-emitted secondary metabolites in mediating plant-soil feedback in a realistic and agricultural context (maize - wheat rotation). I find this article to be an important contribution to the field as the roles played by soil chemical legacies in mediating plant-soil feedbacks have been largely overlooked so far, particularly in the field. I found this manuscript to be extremely well-written and clear. I was impressed by the number of response variables measured by the authors to characterise how wheat plants responded to the soil legacies created by different maize genotypes.
The article presents the results of a plant-soil feedback experiment in which two maize genotypes (wild type or benzoxazinoid-deficient bx1 mutant plant) conditioned field soil for one growing season. Monocultures of each genotype occupied alternate strips in the field. At the end of this conditioning phase, the authors analysed benzoxazinoids in the soil and found that the soil conditioned by WT maize was characterized by greater concentrations of several benzoxazinoids. In fact, most benzoxazinoids were below the detection limit for soil conditioned by bx1 mutant plants. These differences in soil chemical legacies were associated with differences in bacterial and fungal communities in the roots and rhizosphere of maize. Soon after the maize harvest, monocultures of three wheat varieties were grown in soil that was conditioned by either WT or bx1 maize plants. This factorial design allowed the authors to study the response of different wheat varieties to soil legacies created by maize genotypes that differ in their ability to produce and release benzoxazinoids into the soil. Although root and rhizosphere microbial communities were mainly driven by wheat genotype (and not by maize soil conditioning), soil conditioning effects on benzoxazinoid concentrations were still visible at the end of the feedback phase, but only for specific compounds (e.g. AMPO). In comparison to wheat grown on bx1-conditioned soil, the authors found that wheat plants grown on benzoxazinoid-conditioned soil had better emergence and were taller and more productive. In addition, benzoxazinoid soil conditioning reduced infestation by the cereal leaf beetle Oulema melanopus (particularly in one wheat variety) but did not affect weed pressure. The authors also found that wheat grown on benzoxazinoid-conditioned soil had more reproductive tillers, which led to greater grain yield (+4-5%). Grain quality, however, was not affected by maize soil conditioning.I appreciated that the authors carefully interpreted the results of their experiment, although data analysis could be improved to take repeated measures within a plot into account. Overall, this is a compelling study, with rigorous and numerous measurements and state-of-the-art methods in plant/soil ecology. This study is unique in that it demonstrates the important role that soil chemical legacies can play in mediating plant-soil interactions and influencing the fitness of the following crop in a realistic agricultural setting. Therefore, I believe that this work will be of broad interest to plant and soil ecologists, as well as to agronomists.
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Reviewer #2 (Public Review):
Gfeller et al. performed an experiment to test the mechanism underlying plant-soil feedback-induced effects on crop yield using two common rotation partners, corn and wheat, that are grown in sequence with one another in agricultural fields across years. The authors use a benzoxazinoid-deficient corn genotype to show that, compared to soil conditioned in year one by a wild-type (normal) corn variety, wheat growth, and yield decreased in year two. As part of this experiment, the authors also showed that benzoxazinoids exuded from corn roots are persistent over time (i.e., they can be detected in the soil long after corn was harvested), resulting in changes to the structure of bacterial and fungal communities, and reduce insect feeding damage to wheat. These effects were replicated across three different wheat …
Reviewer #2 (Public Review):
Gfeller et al. performed an experiment to test the mechanism underlying plant-soil feedback-induced effects on crop yield using two common rotation partners, corn and wheat, that are grown in sequence with one another in agricultural fields across years. The authors use a benzoxazinoid-deficient corn genotype to show that, compared to soil conditioned in year one by a wild-type (normal) corn variety, wheat growth, and yield decreased in year two. As part of this experiment, the authors also showed that benzoxazinoids exuded from corn roots are persistent over time (i.e., they can be detected in the soil long after corn was harvested), resulting in changes to the structure of bacterial and fungal communities, and reduce insect feeding damage to wheat. These effects were replicated across three different wheat cultivars. Weed pressure (benzoxazinoids have previously been shown to be allelopathic towards other plants) and wheat quality were unaffected in the experiment.
Strengths:
The authors use a large-scale field experiment to test their hypothesis. This is a very important aspect of the study. Most plant-soil feedback studies are conducted using potted plants or, at best, small-plot trials. This experiment was performed using large field plots, which is essential for making reliable inferences about crop rotations and yields in agriculture.
The study does a nice job of testing the underlying chemical mechanisms of how plant-soil feedbacks operate. Many studies have shown that conditioning the soil with one plant species affects the performance of a second plant species sharing that soil, but in virtually all cases we don't know, and can only speculate, what mechanisms are causing this effect.
The data reported are impressive for a few reasons. First, the authors make it a point to measure a wide variety of variables, making the findings particularly robust. I was impressed with the breadth of phenotyping considered by the authors. For example, their plant growth measurements were highly detailed, going from early-season crop performance (e.g., seedling emergence, chlorophyll, height, biomass, water content) to late-season yield effects (e.g., tiller density per plant and unit area, kernel weight) and even considering crop quality (e.g., protein, dough stability), which is usually ignored and assumed to not differ. This was clearly a ton of work! As part of this, they comprehensively measured variables related to plants, insects, weeds, soil microbes, etc., making this highly interdisciplinary work. And a second factor related to the data - the treatment effects were very consistent and impressive in magnitude. While not all variables were significantly affected, the ones that showed effects were consistent and not trivial (i.e., they were biologically significant).
Weaknesses:
While corn and wheat are common rotation partners around the world, it still seems like wheat was an odd choice for this experiment. The main reason I say this is that, as the authors point out, both plants produce benzoxazinoids. This makes it difficult to ascertain the effects of corn-derived benzoxazinoids since wheat is also exuding these compounds from its roots. A non-benzoxazinoid crop like soybean seems like it would've been a better choice since you wouldn't have the confounding effect of both the conditioning and feedback plants producing the same secondary metabolites. On the other hand, the fact that wheat produces benzoxazinoid could be a factor driving its yield response (i.e., crops that don't produce benzoxazinoids may show allelopathic-negative reactions).
The authors show that experimentally eliminating benzoxazinoids has a negative effect on the subsequent crop. While this is interesting from a mechanistic standpoint, it's less compelling than if the reverse was true. In other words, the authors simply show why corn is a good rotation crop for wheat, which has been known for a very long time, even if the mechanism was unclear. The authors argue that this could open the door for breeding that targets benzoxazinoids, which may very well be true; however, the outcomes would be more interesting if the study was showing that existing practices result in low yields and they were paving a path for how to ameliorate this.
In the end, it remains unclear whether the effect is driven by a direct effect from benzoxazinoids on wheat or an indirect effect caused by changes in soil microbes. The authors do a good job of speculating on the likelihood of these two mechanisms in the Discussion; however, they can't say with certainty. They would have to use sterilized soil as a separate treatment to differentiate these mechanisms.
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