Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field‐grown maize roots

Abstract

Different root types of plants are colonized by a myriad of soil microorganisms, including fungi, which influence plant health and performance. The distinct functional and metabolic characteristics of these root types may influence root type-inhabiting fungal communities. We performed internal transcribed spacer (ITS) DNA profiling to determine the composition of fungal communities in field-grown axial and lateral roots of maize (Zea mays) and in response to two different soil phosphate (P) regimes. In parallel, these root types were subjected to transcriptome profiling by RNA sequencing (RNA-Seq). We demonstrated that fungal communities were influenced by soil P levels in a manner specific to root types. Moreover, maize transcriptome sequencing revealed root type-specific shifts in cell wall metabolism and defense gene expression in response to high P. Furthermore, lateral roots specifically accumulated defense-related transcripts at high P levels. This observation was correlated with a shift in fungal community composition, including a reduction in colonization by arbuscular mycorrhizal fungi, as observed in ITS sequence data and microscopic evaluation of root colonization. Our findings suggest soil nutrient-dependent changes in functional niches within root systems and provide new insights into the interaction of individual root types with soil microbiota.

The effects of soil phosphorous content on microbiota are driven by the plant phosphate starvation response

“…All SynCom treatments decreased shoot Pi content in the low Pi conditions compared to 275 the uninoculated plants but recovered to a higher shoot Pi level than the uninoculated treatments upon 276 transferring to high Pi conditions, reproducing our previous report [4] [19,27,29]. Several studies link host physiological response to the soil 290 phosphate status with the bacterial [4,51] and fungal [34,36] microbiome. A recent report of Arabidopsis 291 planted in a 60-year-long annual phosphorus fertilization gradient (the same soil used in the current study) 292 showed a modest P effect on plant microbiome composition [41].…”

“…213The microbial community composition in soil, while governed by its own set of ecological processes [19], 30 has an immense influence on the composition of the plant microbiota [20][21][22]. Correlations with soil 31 microbial diversity, and by derivation, with plant microbiota composition and diversity, were observed for 32 soil abiotic factors such as pH [19,[23][24][25], drought [25][26][27][28][29][30] and nutrient concentrations [19,25,[31][32][33][34][35]. Soil 33 nutrient concentrations, in particular orthophosphate (Pi) -the only form of phosphorous (P) that is 34 available to plants -produce comparatively modest to unmeasurable changes in microbial community 35 composition [35,36].…”

Nitrogen‐dependent bacterial community shifts in root, rhizome and rhizosphere of nutrient‐efficient Miscanthus x giganteus from long‐term field trials

“…It is now well-established that different plant organs, including roots, stalks, leaves, seeds and even flowers recruit different microbial communities in sugarcane, maize, rice, Arabidopsis and grape (Johnston-Monje, Lundberg, Lazarovits, Reis, & Raizada, 2016;Lundberg et al, 2012;Paszkowski & Gutjahr, 2013;De Souza et al, 2016;Zarraonaindia et al, 2015). Furthermore, fungal community distribution even diverged among different parts of the same maize organ, lateral and axial roots (Yu et al, 2018). Filtering of bacterial communities by the rhizosphere and further more strictly by plant organs apparently shapes these different communities (Hardoim, Overbeek, & Elsas, 2008;Reinhold-Hurek et al, 2015).…”

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

“…A similar activation of defence-related genes was observed in field-grown maize when the plants were grown at high soil Pi concentrations. This was accompanied by alterations in the root-inhabiting fungal community and with reduced root-length colonization by AMF (Yu et al, 2018). It appears that lowering plant defences at low Pi serves to increase the chances of recruiting beneficial soil microbes to overcome the nutritional stress.…”