Physiological and molecular mechanisms of improved iron nutrition of peanut intercropping with maize

Abstract

Intercropping is one of the most important farming practices for efficient use of farmland ecosystems and sustainable yield productions. Peanut intercropped with maize could significantly reduce peanut chlorosis symptom and increase the plant iron (Fe) content and crop yield in the North China Plain. The physiological and molecular mechanisms behind this phenomenon have been extensively studied for decades. Peanut and maize have evolved two distinct mechanisms in response to Fe deficiency, known as “the Strategy I” and “the Strategy II”, respectively. The Strategy I plants take up Fe2+ through soil acidification and Fe3+ reduction, while the Strategy II plants acquire Fe via secreting mugineic acid family phytosiderophores (MAs) to dissolve insoluble ferric Fe and to form absorbable Fe(III)–MAs complexes in the rhizosphere. At the molecular level, key genes involved in Fe acquisition have been well characterized. In the Strategy I plants, peanut ferric reductase oxidase2 (AhFRO2) and iron regulated transporter1 (AhIRT1) are responsible for the reduction of Fe(III)-chelate to Fe(II) and the uptake of Fe(II), respectively. In the Strategy II plants, MAs are synthesized from methionine and secreted by mugineic acid transporter1 (MA1). The secreted MAs solubilize Fe in the rhizosphere and the resultant Fe(III)-MAs complex is then absorbed by the yellow stripe1 (YS1) transporter in maize. As a result, the Strategy II maize is more effective at mobilizing precipitated Fe, less affected by high pH and bicarbonate levels, and having a much stronger ability to resist Fe-limitation stress in calcareous soils compared with Strategy I peanuts. However, the Fe-limitation stress in peanuts could be alleviated when intercropping with maize. At physiological and biochemical levels, the ecological advantages of rhizosphere interaction is to significantly enhance the absorption and transport of Fe by intercropped peanut roots and to validate the functions of genes involved. In particular, it has been demonstrated that the AhYSL1 gene which is expressed in the peanut root epidermal cells can specifically regulate the absorption of the Fe(III)–DMA compound. Peanuts could directly absorb Fe(III)-DMA from the rhizosphere of intercropped maize. The intercropping of maize and peanut with different Fe absorption mechanisms not only improves peanut Fe nutrition but also increases resistance of these two crops. In addition, higher accumulation of photosynthesis-related proteins in intercropped peanut leaves suggests that the intercropped peanuts have a higher photosynthetic efficiency. Moreover, stress-responsive proteins displayed elevated expression levels in both peanut and maize in a monocropping system. This suggests that intercropping contributes to resistance to stress conditions. Intercropping also enhances jasmonate signaling and weakens ethylene signaling in peanut and maize roots, which may improve ecological adaptation of the maize and peanut plants in the intercropping system. The advantage in ecology system makes maize/peanut intercropping as a typical model of “bio-fortification”. The nutrient benefit of the inter-rhizosphere regulatory measure can be an important technological measure for bio-fortification to improve human health and nutrition. The research on the mechanisms underlying the beneficial effects of maize/peanut intercropping could provide important theoretical and applied bases to understand and utilize the reciprocal effect of different plant biological characteristics and to improve rhizosphere ecological environments, crop iron nutrition and efficient utilization of resources.