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

Abstract

Key findingOur data illustrates for the first time that root type identity and phosphate availability determine the community composition of colonizing fungi and shape the transcriptomic response of the maize root system.SummaryPlant root systems consist of different root types 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 L.) and in response to two different soil phosphate (P) regimes. In parallel, these root types were subjected to transcriptome profiling by RNA-Seq.We demonstrated that fungal communities were influenced by soil P levels in a root type-specific manner. Moreover, maize transcriptome sequencing revealed root type-specific shifts in cell wall metabolism and defense gene expression in response to high phosphate. 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 of colonization by arbuscular mycorrhiza fungi as observed in ITS sequence data and microscopic evaluation of root colonization.Our findings point towards a diversity of functional niches within root systems, which dynamically change in response to soil nutrients. Our study provides new insights for understanding root-microbiota interactions of individual root types to environmental stimuli aiming to improve plant growth and fitness.

Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation

“…Interactions between roots and their rhizosphere microbiota are essential for plant growth and performance 7,8 . It is known that dynamic patterns of the root transcriptome synchronize with distinct microbial taxa colonizing different root types 26,27 . However, numerous scenarios and mechanisms by which microbes modulate plant development are still unknown especially in crops 44 .…”

“…The great architectural and functional diversity of the maize root system has the potential to shape the rhizosphere microbiota composition 25 . Specifically, root type-specific metabolic properties influence microbial communities inhabiting respective root types in maize and rice [26][27][28] . Conversely, it has been suggested that rootassociated bacteria contribute to differential nitrogen use efficiencies observed in indica and japonica rice varieties 29 , suggesting that root microbiota could alleviate overall nutrient stress in crops.…”

Prioritizing host phenotype to understand microbiome heritability in plants

“…Relatively few studies have investigated spatial microbiome dynamics within organs, even fewer while also considering host genotype. In maize, fungal colonization differed between axial and lateral roots, corresponding to physiological and transcriptional differences (Yu et al ., 2018). Similarly, Avena fatua rhizosphere communities varied in density and composition along the length of individual roots, matching spatial patterns in exudate content (DeAngelis et al ., 2009).…”

Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems

“…Drought-induced expression changes that were tied to fitness under drought suggested that plants may respond adaptively to water limitation and concomitant P deficiency by intensifying interactions with AM fungi. Our hypothesis based on these patterns and on previous studies of plant relations with AM fungi (Colard et al, 2011; Lanfranco et al, 2018; Mbodj et al, 2018; Yu et al, 2018), that interactions with AM fungi could have positive fitness consequences under drought, held up in the next dry season. We found that root interactions with AM fungi were positively linked with straw biomass, an important fitness component, within dry as well as between wet and dry field conditions.…”

“…Two published examples provide excellent insights that are extended by our study. In the first, Yu and colleagues measured gene expression in roots of field-grown maize at high and low soil phosphate levels, observing that genes involved in signaling and cell wall metabolism were particularly responsive (Yu et al, 2018). In the second, Kawakatsu and co-workers measured gene expression in both the roots and shoots of a panel of diverse rice accessions grown in relatively dry upland growth conditions (Kawakatsu et al, 2021).…”