The mycorrhizal colonization by Funneliformis mosseae preferentially improves drought stress tolerance in roots of sensitive parental maize inbreed plants: phenomics and metabolomic pathway analysis

Drought is a major constraint for maize cultivation, while arbuscular mycorrhizal fungi (AMF) may alleviate its negative impact in a genotype-dependent manner. Here, we cultivated plants from two inbred lines (drought-tolerant K1, drought-sensitive K2) and their hybrids (KH) with or without Funneliformis mosseae colonization under well-watered and drought conditions, for integrating phenotyping, biomass parameters and transcriptomic data.

Results KH plants exhibited moderate mid-parent heterosis (MPH) in biomass under optimal water, which was increased under drought stress but decreased with AMF colonization. In roots, drought strongly elevated MPH (291%), which was reduced by colonization (80.5%). K1 plants showed moderate drought tolerance, while K2 plants were highly sensitive, yet AMF induced a remarkable 15-fold root expansion in K2 plants under drought.

KH plants tolerated drought but responded little to colonization, whereas AMF stimulated ear formation in K1 plants. Transcriptomic analysis revealed genotype-specific reprogramming that paralleled these phenotypes. In K1 plants, drought and AMF stabilized the expression of photosynthetic genes (PSI, PSII, LHCb, Calvin-cycle), correlating with biomass maintenance, and activated CYP450 71A1 and CONSTANS-like 3, consistent with auxin metabolism and flowering stimulation.

In K2 plants, strong repression of photosynthesis genes and induction of indole- 3-acetaldehyde oxidase, auxin-binding protein 1, coronatine-insensitive 1 and tasselseed-2 reflected its drought sensitivity, hormone-driven root plasticity, and altered reproductive development under AMF. In KH plants, selective reprogramming of expression of photosynthetic genes, including ~12-fold induction RbcX gene, simultaneous activation of 13 heterosis-related genes, coincided with biomass stability, heterosis, and consistent flowering, with only limited AMF modulation of hormonal pathways.

Conclusion Our findings demonstrate that AMF enhances drought resilience in a genotype-dependent manner, linking phenotypic responses with transcriptomic regulation of photosynthesis, hormone signaling, and flowering. AMF primarily improved root plasticity and hormone- dependent stress adaptation in the drought-sensitive K2 plants, stabilized photosynthesis and reproductive development in tolerant K1 plants, while the KH hybrid plants the AMF colonization combined biomass stability with distinct transcriptional adjustments.

These results provide insight into how AMF contributes to maize performance under water limitation and highlight the importance of genotype-specific interactions.