Perenniality, more than genotypes, shapes biological and chemical rhizosphere composition of perennial wheat lines

Perennial grains provide various ecosystem services compared to the annual counterparts thanks to their extensive root system and permanent soil cover. However, little is known about the evolution and diversification of perennial grains rhizosphere and its ecological functions over time. In this study, a suite of -OMICSs - metagenomics, enzymomics, metabolomics and lipidomics - was used to compare the rhizosphere environment of four perennial wheat lines at the first and fourth year of growth in comparison with an annual durum wheat cultivar and the parental species Thinopyrum intermedium. We hypothesized that wheat perenniality has a greater role in shaping the rhizobiome composition, biomass, diversity, and activity than plant genotypes because perenniality affects the quality and quantity of C input - mainly root exudates - hence modulating the plant-microbes crosstalk. In support of this hypothesis, the continuous supply of sugars in the rhizosphere along the years created a favorable environment for microbial growth which is reflected in a higher microbial biomass and enzymatic activity. Moreover, modification in the rhizosphere metabolome and lipidome over the years led to changes in the microbial community composition favoring the coexistence of more diverse microbial taxa, increasing plant tolerance to biotic and abiotic stresses. Despite the dominance of the perenniality effect, our data underlined that the OK72 line rhizobiome distinguished from the others by the increase in abundance of Pseudomonas spp., most of which are known as potential beneficial microorganisms, identifying this line as a suitable candidate for the study and selection of new perennial wheat lines.

Automated summary

Perennial grains, with their extensive root system and permanent soil cover, provide various ecosystem services compared to annual grains. However, the evolution and diversification of the rhizosphere and its ecological functions over time are not well understood. In this study, a suite of -OMICSs was used to compare the rhizosphere environment of four perennial wheat lines at different growth stages. The results showed that wheat perenniality played a greater role in shaping the rhizobiome composition, biomass, diversity, and activity than plant genotypes. The continuous supply of sugars in the rhizosphere created a favorable environment for microbial growth, resulting in higher microbial biomass and enzymatic activity. Changes in the rhizosphere metabolome and lipidome over the years led to the coexistence of more diverse microbial taxa and increased plant tolerance to stresses.