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.
Highlights
Phosphorus (P) is one of the macronutrients essential for plant growth and productivity, on a global scale it is a slowly disappearing nutrient and unlike some finite resources like oil, for which alternatives can be found, there are currently no substitutes for P fertilizers [1,2]
arbuscular mycorrhizal (AM) host plants possess specific Pi transporters from the PHT1 family targeted to the periarbuscular membrane (PAM), which actively transport Pi delivered by the fungus to host cells [13,14,15]
The expression of plant Pi transporter genes involved in mycorrhizal Pi uptake (MPU) is locally and cell -autonomously controlled during AM fungal colonization of root cortical cells [18,19,20] and is tightly regulated by transcription factors which bind to distinct cis-regulatory elements present in respective gene promoters [21,22,23]
Summary
Phosphorus (P) is one of the macronutrients essential for plant growth and productivity, on a global scale it is a slowly disappearing nutrient and unlike some finite resources like oil, for which alternatives can be found, there are currently no substitutes for P fertilizers [1,2]. Most land plants, including important crops like maize, form arbuscular mycorrhizal (AM) symbiosis with soil based fungi from the subphylum Glomeromycotina [4,5] in response to Pi limitation. AM host plants possess specific Pi transporters from the PHT1 family targeted to the PAM, which actively transport Pi delivered by the fungus to host cells [13,14,15] This pathway of soilderived mineral P uptake is known as the mycorrhizal Pi uptake (MPU) pathway, which can operate exclusively or in parallel to direct Pi uptake (DPU) from the soil solution across the root epidermis [16]. The expression of plant Pi transporter genes involved in MPU is locally and cell -autonomously controlled during AM fungal colonization of root cortical cells [18,19,20] and is tightly regulated by transcription factors which bind to distinct cis-regulatory elements present in respective gene promoters [21,22,23]
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