Neighboring plants divergently modulate effects of loss-of-function in maize mycorrhizal phosphate uptake on host physiology and root fungal microbiota

Abstract

Maize, a main crop worldwide, establishes a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi providing nutrients to the roots from soil volumes which are normally not in reach of the non-colonized root. The mycorrhizal phosphate uptake pathway (MPU) spans from extraradical hyphae to root cortex cells housing fungal arbuscules and promotes the supply of phosphate to the mycorrhizal host in exchange for photosynthetic carbon. This symbiotic association with the mycobiont has been shown to affect plant host nutritional status and growth performance. However, whether and how the MPU affects the root microbial community associated with mycorrhizal hosts in association with neighboring plants, remains to be demonstrated. Here the maize germinal Mu transposon insertion mutant pht1;6, defective in mycorrhiza-specific Pi transporter PHT1;6 gene, and wild type B73 (wt) plants were grown in mono-and mixed culture and examined under greenhouse and field conditions. Disruption of the MPU in pht1;6 resulted in strongly diminished growth performance, in reduced P allocation to photosynthetic source leaves, and in imbalances in leaf elemental composition beyond P. At the microbial community level a loss of MPU activity had a minor effect on the root-associated fungal microbiome which was almost fully restricted to AM fungi of the Glomeromycotina. Moreover, while wt grew better in presence of pht1;6, pht1;6 accumulated little biomass irrespective of whether it was grown in mono-or mixed culture and despite of an enhanced fungal colonization of its roots in co-culture with wt. This suggested that a functional MPU is prerequisite to maintain maize growth and that neighboring plants competed for AM fungal Pi in low P soil. Thus future strategies towards improving yield in maize populations on soils with low inputs of P fertilizer could be realized by enhancing MPU at the individual plant level while leaving the root-associated fungal community largely unaffected.

Maize Field Study Reveals Covaried Microbiota and Metabolic Changes in Roots over Plant Growth

“…We found that the root lipid status between wild-type and AMF-deficient pht1 ; 6 plants differed more strongly under NK than under NPK conditions, which is likely linked to perturbed cross-kingdom lipid transfer from the host to AMF in the mutant roots. We also observed that the performance of pht1 ; 6 mutants was reduced compared to that of the wild type, as previously shown ( 40 , 60 ), and more severely at the vegetative growth phase. These performance differences were partially compensated for at the reproductive growth phase under P-sufficient conditions (NPK).…”

The genetic architecture of adaptation to leaf and root bacterial microbiota inArabidopsis thaliana

“…In addition, because the relative effect of host genetics on the microbiota can highly depend on the plant habitat, in particular the inoculum source (e.g. agricultural soil) (Robertson-Albertyn et al 2017; Hubbard et al 2018; Fabiańska et al 2020), setting up genetic association studies in a common garden can bring to partial conclusions on the host genetics controlling for microbiota (Oyserman et al 2020). One approach to tackle these issues is to conduct Genome-Environment Association (GEA) analysis.…”

Shift in beneficial interactions during crop evolution

“…Fourth, our current understanding on plant–plant interactions mediated by microorganisms is still very limited. A recent study suggests that maize plants trigger AM fungal colonization in mutant neighboring plants displaying deficiency in the mycorrhizal Pi uptake pathway, through nutrient delivery to the CMN (Fabianska et al, 2020 ). This example opens interesting perspectives for the selection of genotypes that invest in the CMN.…”