Influence of root cortical aerenchyma on the rhizosphere microbiome of field-grown maize

Abstract

The root anatomical phenotype root cortical aerenchyma (RCA) decreases the metabolic cost of soil exploration and improves plant growth under drought and low soil fertility. RCA may also change the microenvironment of rhizosphere microorganisms by increasing oxygen availability or by reducing carbon rhizodeposition. We tested the hypothesis that plants with contrasting expression of RCA have different rhizosphere prokaryotic communities. Maize inbreds were grown in two field sites, Limpopo Province, South Africa and Pennsylvania, USA, and their rhizosphere soil sampled at flowering. High- and low-nitrogen fertilization was imposed as separate treatments in the experiment in South Africa. The rhizosphere microbial composition of plants with contrasting RCA was characterized by metabarcoding of the 16S rRNA genes. Geographic location was the most important factor related to the composition of rhizosphere microbial communities. In the site in South Africa, RCA explained greater percent of variance (9%) in the composition of microbial communities than genotype (7%). Although other root anatomical and architectural phenotypes were studied as possible cofactors affecting the microbial composition, RCA was among the best significant explanatory variables for the South African site although it was neutral in the Pennsylvania site. High-RCA rhizospheres significantly enriched OTUs of the families Burkholderiaceae (in South Africa) and Bacillaceae (in USA), compared to low-RCA plants, and OTUs of the families Beijerinckiaceae and Sphingomonadaceae were enriched at the two nitrogen levels in high RCA plants in South Africa. Our results are consistent with the hypothesis that RCA is an important factor for rhizosphere microbial communities, especially under suboptimal nitrogen conditions.

Root phenotypes for improved nitrogen capture

“…How these rhizosphere processes are associated with microbes participating in the nitrogen cycle remains elusive. The relative abundance of ammonia oxidizing Archaeans of the genus Nitrososphaera was significantly associated with high RCA expression under low nitrogen conditions in field grown maize (Galindo-Castañeda 2018;Galindo-Castañeda et al 2023). These results suggest that maize with more RCA may favor nitrification, perhaps through the transport of oxygen to the rhizosphere using the RCA channels, similarly to rice (Li et al 2008).…”

“…Root-microbe associations in the rhizosphere could play an important role in plant nitrogen uptake given that microbes harness a wide range of enzymes that catalyze the transformation of nitrogen-containing compounds in soils (Kuypers et al 2018) and because microbes participate in the regulation and activity of nitrogen transport from the rhizosphere to the root cortex (Zhang et al 2019;Hui et al 2022). Recent research has demonstrated that root architecture (Yu et al 2021) and anatomy (Salas-González et al 2021, Galindo-Castañeda 2018, Galindo-Castañeda et al 2023) interact with rhizosphere microbes under low nutrient supply, but the mechanisms and relevance of the activity of nitrogen cycling microbes and their associations with adaptive root anatomical and architectural phenotypes in crops is poorly understood. Synergies and tradeoffs of microbial associations as influenced by root anatomy and architecture to optimize nitrogen capture by crops in agroecosystems are promising avenues for crop breeding and microbiome engineering (Galindo-Castañeda et al 2022).…”

Rhizosphere engineering for semiarid tropics: prospects and bottlenecks

“…These traits can be targeted through plant breeding programs to develop new cultivars suited for the challenges of modern agriculture. However, it is crucial to ensure that the selection for these traits does not compromise beneficial microbial associations in the rhizosphere, as these associations are essential for sustainable crop production [80]. The selection of plants for rhizosphere improvement is vital for enhancing plant growth and productivity and for environmental remediation.…”