Maize genotypes foster distinctive bacterial and fungal communities in the rhizosphere

Maize possesses exceptional diversity and undergoes rapid and extensive genetic changes during breeding. New genotypes impact soil microbiota, and respond differently to current climates compared with older genotypes in diverse environments, assessment of such interactions was a key novelty of the present study. Here, we investigated associations between genetic relationship, plant traits and soil bacterial and fungal composition based on six decades of maize breeding in China. Soil microbiome of six maize cultivars, each representing a popular variety developed each decade from the 1950s to 2000s, were collected from a long-term field experiment (established in 2012) and a pot experiment. Microbial community shifts were deduced from the taxonomic co-occurrence and co-exclusion network dynamics across maize growth stages. As expected, cultivar replacement influenced the soil bacterial and fungal composition (P < 0.001). At flowering, different maize genotype groups had distinctive bacterial community structure in the rhizosphere and root-zone soil. Aboveground dry matter, plant height and leaf area were plant traits that best explained the bacterial community variance (29.0 % in rhizosphere and 19.3 % in root-zone soil; P = 0.01) among maize cultivars. Specific root length showed a negative correlation with the gene copy numbers of α-Proteobacteria. The major maize cultivar from the 2000s (M00s) had relatively more cultivar-enriched bacterial taxa, with a greater proportion of the genera Acidibacter and Variibacter in root-zone soil. Furthermore, the M00s cluster contained the most phoD-genes related to phosphorus cycling at harvest, and had the highest bacteria/fungi ratio in the root zone at elongation and flowering. The predominant taxa in the biggest module changed with cultivar replacement, from Proteobacteria in the older maize cultivars to Acidobacteria in the M00s cultivar. The contemporary M00s cultivar may attract beneficial bacteria and fungi while reducing contact with other fungi, which improves soil nitrogen and phosphorus availability. If the plant-associated microbiome could serve as an extended phenotype, then specific gene locus in the maize genome could be targeted to optimize maize breeding for sustainable farming systems.