How the rhizosphere microbiome can sustainably improve nutrient efficiency and productivity in intercropping

How the rhizosphere microbiome can sustainably improve nutrient efficiency and productivity in intercropping
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Humanity must solve several fundamental challenges in the near future. One challenge is how to feed an ever-growing population. Another challenge is how to make agriculture ecologically more sustainable to reduce pesticide and artificial fertilizer release into the environment. Our study tackles both of these challenges. We focus on intercropping, the simultaneous cultivation of multiple crops on the same field, which is typically associated with higher resource use efficiency, pathology control, yield and ecological sustainability. However, the exact mechanism by which these benefits arise and the role of the rhizosphere microbiome in this process remain generally unknown.

The peanut and maize intercropping offers an effective and sustainable way to ensure iron and zinc biofortification to prevent hidden hunger

Since 2000, it is known that peanut/maize intercropping improves iron nutrition via direct belowground facilitation involving root exudates1-4 (Fig. 1). Higher plants show two alternative iron deficiency-induced molecular and physiological responses1-3. Peanut follows strategy I (dicots and non-graminaceous monocots) and directly reduces Fe(III) to Fe(II), followed by Fe(II) absorption1-3. In contrast, maize follows strategy II (graminaceous monocots) and secretes phytosiderophores of the mugineic acid family (MAs) to chelate insoluble Fe(III) followed by MAs-Fe(III) complex absorption1-3. Maize outperforms peanut in iron acquisition in alkaline soils because strategy II is less sensitive to high pH1-3. It was proposed that intercropping benefits peanut because it enhances deoxymugineic acid (DMA) secretion from maize root, which solubilizes more Fe(III) in the soil and is then absorbed as DMA-Fe(III) complex by nearby peanut plants3-4. However, this current plant-plant interaction model for iron utilization does not integrate interactions of plants with the root-microbiome. We hypothesize that peanut/maize intercropping could modulate the rhizosphere microbiome through the proximity of plant roots, which in turn could promote the mixing of root exudates, microbiome members, and their iron-chelating siderophores and thus improve iron acquisition opportunities.

Fig. 1 | Phenotype and mechanism based on root-root interaction of peanut iron improvement by intercropping with maize grown in calcareous soil. a. Filed and pot phenotype of monocropping peanut suffering from iron-deficiency and peanut iron nutrition improvement by intercropping with maize. b intercropping peanut utilizes Fe chelated by phytosiderophore mugineic acids (MAs).

The rhizosphere microbiome is essential to improve iron nutrition of crops in intercropping, as shown by experiments combining microbiome profiling, strain and substance isolation and functional validation

By sterilizing soil and conducting pot experiments in the greenhouse, we show that the rhizosphere microbiome is essential to improve peanut iron nutrition in intercropping. Specifically, intercropping induced both a shift and convergence in the rhizobacteria composition between plant species. We discovered that the genus Pseudomonas was cross-enriched from maize to peanut, and emerged as a key player associated with iron nutrition improvement. We characterized the representative rhizosphere isolate P. extremorientalis 1502IPR-01 and demonstrated that this isolate produces the siderophore pyoverdine, which solubilizes iron from soil, making it available for plant and microbial metabolism. Moreover, we managed to harness this isolate for agricultural application in greenhouse and field experiments and show that the addition of this probiotic isolate suffices to efficiently improve iron nutrition and yield in crops.

Fig 2 | Model of how peanut/maize intercropping enriches for Pseudomonas spp. in the rhizosphere to improve iron nutrition via secreting siderophore pyoverdine.

The promising approach of identifying key functional microorganisms and microbial metabolites that contribute to the increase in nutrient efficiency and crop yield by intercropping

In summary, we elucidated a mechanism of how intercropping benefits plants through rhizosphere microbiome convergence (Fig. 2). Our study highlights that the benefit of intercropping from belowground facilitation leads to a gained function for peanut through a cross-enrichment of rhizosphere microbiome members obtained from maize (Fig. 2). Our findings offer applied opportunities for a probiotic treatment to improve plant health and crop yield in situations where intercropping is not possible. While we have identified a probiotic strain and its secreted beneficial compound, there is great potential to further improve the process through bioengineering. Our mechanistic insights on iron nutrition improvement might be a general phenomenon and should thus be tested in other intercropping systems with different plant combinations to increase both yield and sustainability. Our results further show how detailed knowledge of inter-kingdom interaction mechanisms helps to develop ecologically sustainable agriculture and food security.

Referennces

  1. Zuo, Y. M., Zhang, F. S., Li, X. L. & Cao, Y. P. Studies on the improvement in iron nutrition of peanut by intercropping with maize on a calcareous soil. Plant and Soil 220, 13–25 (2000).
  2. Zuo, Y. & Zhang, F. Iron and zinc biofortification strategies in dicot plants by intercropping with gramineous species. A review. Agronomy for Sustainable Development. 29, 63–71 (2009).
  3. Dai, J. et al. From leguminosae/gramineae intercropping systems to see benefits of intercropping on iron nutrition. Frontiers in Plant Science. 10, 605 (2019).
  4. Xiong, H. et al. Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant Cell & Environment. 36, 1888–1902 (2013).

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Agricultural Biotechnology
Life Sciences > Biological Sciences > Agriculture > Agricultural Biotechnology
Microbiome
Life Sciences > Biological Sciences > Microbiology > Microbial Communities > Microbiome
Plant Ecology
Life Sciences > Biological Sciences > Ecology > Plant Ecology
Plant Biotechnology
Life Sciences > Biological Sciences > Plant Science > Plant Biotechnology

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