However, not all the graminaceous could correct the Fe nutrition of partners. The leaves of citrus and peanut did not recover from Fe deficiency chlorosis intercropped with ys3 maize mutant plants, which is unable to release phytosiderophores Cesco et al. It seems that a complementary strategy is necessary to increase the Fe nutrition of Strategy I plants in intercropping systems. The interactions in the rhizosphere affect biogeochemical cycling and nutrient availability, which affect plant growth and tolerance to biotic and abiotic stress Philippot et al.
The interactions between plant roots and the rhizosphere microbiome are critical for improving plant fitness Zhalnina et al. Plant can secret different exudates to rhizosphere affected by environmental factors such as plant growth, nutrient availability and microorganisms Mimmo et al.
Materials and Methods
The root exudates including primary metabolites sugars, amino acids, and organic acids can shape the rhizosphere microbiome Badri and Vivanco, In turn, the associated microorganisms can influence plant health and growth Huang et al. The soil microorganisms have a significant effect on nutrient availability for plants in the rhizosphere Mimmo et al. The microorganisms can quickly utilize root exudates which affects plant nutrient foraging Alegria Terrazas et al.
Inoculation with plant growth-promoting rhizobacteria showed potential in benefiting the efficiency of nutrient acquisition of root Pii et al. The effects of intercropping systems on soil physicochemical and biochemical characteristics are complicated due to differences among species Ladygina and Hedlund, In typical intercropping systems, legumes benefit soil quality by increasing soil carbon and nitrogen sequestration Cong et al.
Furthermore, the soil urease and phosphomonoesterase activities were also improved by intercropping Li et al.
Another field experiment showed that the pH and soil available phosphorus Olsen-P concentration in the rhizosphere of peanut crops decreased in the intercropping system after the vegetative stage Guo et al. However, in seven cucumber intercropping systems, intercropping had no significant effects on physicochemical characteristics such as soil moisture, pH, and the electrical conductivity in two growing seasons Li and Wu, Facing Fe-limited conditions, Strategy I and II plants secrete different compounds into the rhizosphere to facilitate Fe uptake Chen et al.
Iron Nutrition in Plants and Rhizospheric Microorganisms
The phenolic compounds, such as coumarins and flavins, secreted by Strategy I plants not only mobilize insoluble Fe but also affect the root microorganisms to promote plant health Siso-Terraza et al. Different species can secrete different coumarins to better adapt to their environments Rajniak et al. Secondary metabolites secreted from roots including antibiotics and volatiles play a key role in the performance of bacteria Schulz-Bohm, However, the directly effect of secondary metabolites on plant nutrient foraging is barely understood.
They not only alter the root-associated microbiota and suppress herbivore performance but also facilitate the Fe uptake of maize.
Iron Nutrition in Plants and Rhizospheric Microorganisms
The phytosiderophores released by graminaceous species are chelators with high affinity for ferric Fe, and can contribute to the diffusion of Fe in soil Ma, ; Kobayashi and Nishizawa, The available Fe concentration in the rhizosphere of intercropped peanut was significantly higher than that of monocropped peanut Guo et al. The siderophore pyoverdine secreted by Pseudomonas fluorescens was beneficial to the Fe nutrition and growth of Arabidopsis in Fe-limited conditions Trapet et al. Intercropping facilitated nitrogen transfer from soybeans to maize on co-inoculation with AMF, as shown by 15 N labeling Wang et al.
Bacillus subtilis GB03 and Azospirillum brasilense showed a positive effect on Fe nutrition of Arabidopsis and cucumber, respectively Zhang et al. But about their abundance change in intercropping was rarely reported. How the plants shape their root microbiome and the effect of the specific root exudates under Fe deficiency need to be investigated. The role of microorganisms in the Fe nutrition of plant is also not fully understood.
The microorganisms can increase soluble Fe in soil by decreasing soil pH through nitrification and secreting siderophores, which may be also helpful for the Fe nutrition of plant Mimmo et al.
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On another hand, microorganisms are competitive for Fe Mimmo et al. In intercropping systems, more attention was paid on the effect of microorganisms on N and P turnover. Understanding the difference of effect between graminaceous and non-graminaceous on rhizosphere microbiome and their corresponding function differences can provide a new perspective for explaining the rhizosphere process in intercropping system. Knowing how the rhizosphere facilitates interactions in intercropping systems could help us to optimize plant performance by engineering the plant rhizosphere.
In other cases, only the phenomenon was raised. Arachis hypogaea iron-regulated transporter 1 AhIRT1 was the first iron-related transporter to be isolated from the peanut. Ding et al. In other studies, the expression of AhIRT1 was downregulated in intercropped peanut during the reproductive stage Xiong et al. Further work must examine whether the intercropping interactions have a specific effect on the expression of AhIRT1. The expression of AhFRO1 Arachis hypogaea ferric reductase oxidase 1 , which encodes a Fe III -chelate reductase, was affected by the growth stage in intercropping systems.
During the vegetative growth of maize, AhFRO1 was upregulated in intercropping systems while peanut was already in reproductive stage. During this period, monocropped peanut did not show Fe deficiency chlorosis. Subsequently, AhFRO1 was downregulated in intercropping systems owing to the better Fe nutrition status. The ferric reductase activity of peanut roots showed a similar tendency, and was higher during the vegetative growth stage and lower during the reproductive growth stage of maize Guo et al.
The phytosiderophores secreted by maize chelate and solubilize Fe from the rhizosphere, and this is enhanced by specific intercropping interactions Xiong et al. The enhanced amino acid metabolism may increase the release of phytosiderophores in maize roots. Homocysteine S-methyltransferase HMT2 and serine acetyltransferase SAT1 are directly associated with the methionine metabolism pathway. The phytosiderophore-Fe III complex can be absorbed across the plasma membrane of roots by the peanut transporter protein AhYSL1 Arachis hypogaea yellow stripe1-like , a homolog of maize yellow stripe 1 Xiong et al.
Several studies have indicated that intercropping also had a positive effect on the expression of AhYSL1 , especially during the reproductive stage Xiong et al. Further work must examine whether the expression of AhYSL1 is correlated with the phytosiderophores in the rhizosphere. The soil pH and Olsen-P concentration decreased in reproductive stage under the effect of intercropping, while the available Fe concentration was the highest in rhizosphere Guo et al.
It seems that beneficial effects differ during the vegetative stage owing to dynamic changes in the rhizosphere. However, how the other factors that can influence Fe bioavailability such as rhizospheric organic compounds and the microbiome changes along with growth phase indicates that it is still an open question. Reproductive stage is a critical period of plant development which associates with sink formation Marschner, The more nutrient demands in critical period of maize might drive the more release of phytosiderophores, which might induce the expression of AhYSL1.
Phytosiderophores are a class of Fe chelators that enhance adaption in the natural environment; these commonly exist in grasses, but not exclusively. Suzuki et al. As mentioned above, intercropping with purple false brome and barley improved the Fe nutrition of olive trees. In addition, analyzing the function of phytosiderophores can help us to exploit the application of their analogs in agriculture.
The further research need be taken in other intercropping systems to see if these cases can be Fe biofortification by intercropping. The driving factors of rhizosphere changes is an important task if one aims at fully understand the biological and ecological mechanism how intercropping system affect Fe turnover. The previous works in intercropping system have provided different insights to uncover the effects and mechanisms of intercropping systems on Fe nutrition.
Due to the interspecies facilitation of the rhizosphere, especially between Gramineae and Leguminosae, the intercropping systems show more benefits in resource-limited agricultural system including enhancing Fe nutrition. However, we still do not know how plant-microorganisms interactions regulate Fe uptake of root. The microbiome is an essential part to elucidate rhizosphere process in intercropping system. Based on the links between molecular biology and field practices, it will contribute to a universal guide on correcting Fe deficiency chlorosis in different crops with low-input.
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JD summarized and wrote the manuscript. HN and YZ revised the manuscript. YZ provided funding for this work as corresponding author. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Alegria Terrazas, R. Plant-microbiota interactions as a driver of the mineral turnover in the rhizosphere. Badri, D.
Regulation and function of root exudates. Plant Cell Environ.
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Bakker, P. The soil-borne legacy. Cell , — Bavaresco, L.
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