Orientation-driven photosynthesized carbon belowground mediates intercropped peanut microbiota changes for pathogen resistance

Abstract

Abstract Background and Aims Intercropping is a widely used agricultural practice to maintain agri-ecosystem function in intensive farmland. However, traditional combinations of tall and short plants in intercropping systems often sacrifice the health and productivity of short crops due to the planting orientations. Understanding how orientation-driven light intensity vertically allocate photosynthesized carbon and manipulate rhizosphere microbiota of short crops would benefit for the optimization of aboveground design to make use of the belowground microbiota for short plant health in diversified cropping systems. Methods In this study, we manipulated the legume and grass (peanut and maize, respectively, representing short and tall crops) row orientation (east‒west vs. north‒south) in an filed intercropping system and combined high-throughput sequencing and DNA stable isotope probing (DNA-SIP) technology to explore how intercropped orientation-driven photosynthesized carbon synthesis and allocation trigger peanut rhizosphere microbiota for pathogen antagonism. Results From field observations, we found that planting in the north-south orientation enhanced peanut photosynthesized carbon synthesis by up to 2.16 times in terms of photosynthetically active radiation compared to the east‒west orientation in situ. Using DNA-SIP technology, we demonstrated that high light intensity induced 192% more photosynthesized carbon to be released along the plant–root–rhizosphere axis. This released rhizosphere carbon selectively enriched the beneficial microorganism Burkholderia, which effectively suppressed the peanut pathogenic fungus Alternaria alstroemeriae in vitro to promote host plant growth. Conclusion Changing the orientation of intercropping can adjust the distribution of photosynthesized carbon in the rhizosphere by changing the light interception of crops. Peanuts will intercept more light in the north-south direction, resulting in more photosynthesized carbon being allocated to the peanut rhizosphere. These carbon contribute to the assembly of microbiota beneficial to peanut growth and pathogen resistance.