Microbiome Extended Phenotypes Lab
Rewilding the Maize Microbiome to Improve Sustainability?
Modern agriculture has dramatically increased crop productivity, but this progress has often come at the cost of plant–microbiome interactions that contribute to nutrient cycling and ecosystem sustainability. We previously found that domestication and breeding altered the maize rhizosphere microbiome, including microbial functions associated with nitrogen loss (see research highlights below). In this Science Advances paper, we ask whether these lost microbiome-associated traits can be restored by reintroducing genetic variation from maize’s wild ancestor, teosinte.
Using near-isogenic maize lines containing teosinte introgressions, we identified plant genetic regions associated with rhizosphere microbiome functions that suppress nitrification and denitrification, two microbial processes that contribute to nitrogen loss from agricultural soils. These introgressions altered root exudate chemistry and, in turn, changed the composition and function of the rhizosphere microbiome. We further identified candidate plant loci and root exudate metabolites associated with these effects and demonstrated their functional activity in vitro.
Together, our results show that plant genetics can influence microbiome functions with consequences for ecosystem-level nitrogen cycling. More broadly, this work demonstrates that traits lost during crop domestication and breeding may be recoverable from ancestral germplasm. Reintroducing these plant–microbiome interactions provides a potential pathway for developing crops that work with, rather than independently of, the soil microbiome to improve nutrient use and agricultural sustainability.
Have we unknowingly altered the Maize Microbiome interaction?
Plant hosts selectively filter microorganisms that colonize their rhizosphere. This selective process is heritable across plant cultivars, yet the implication of this selection on rhizosphere microbiome function has been relatively unexplored. In modern agriculture, microbiome functions that contribute to crop growth and sustainability have been replaced with agronomic management practices, and the development of modern crop germplasm has been carried out without consideration of the plant microbiome and its functions as an extended phenotype of the crop genome. As time machines are currently not available to explore long-term temporal changes, we had to think creatively to tackle our questions. Inspired by ecological chronosequence studies in soils, forests, and plant communities, we decided to construct a germplasm chronosequence of maize lines that spanned the time period of development ranging from 1949 to 1986. This was possible because of the Plant Variety Protection Act and the outstanding maize germplasm preservation work by the National Plant Germplasm System and the Germplasm Resource Information Network (GRIN). We hoped that our selected lines acted as a genotypic time capsule of the extended microbiome phenotype selected by the historic agronomic breeding environment. This time frame was selected as it covers the introduction and increased usage of synthetic N-fertilizers and advances in maize breeding.
In our paper, we found that genetic relatedness of the host plant and the decade of germplasm development were significant factors in the recruitment of the rhizosphere microbiome. More recently developed germplasm recruited fewer microbial taxa with the genetic capability for sustainable nitrogen provisioning and larger populations of microorganisms contributing to N losses.
While these results are interesting, they present an alarming problem: our study broadly indicates that the development of high-yielding varieties and agronomic management approaches of industrial agriculture has inadvertently modified interactions between maize and its microbiome. Our agricultural practices have unintentionally altered the ecology of maize roots – alterations that appear to have resulted in a potentially less sustainable outcome. What other important ecologically sustainable traits might we have inadvertently altered with good intentions in mind, and are they contributing to our current global climate crisis?
Hopefully, this study can highlight these problems and act as a starting point to create more sustainable agricultural systems with a microbe-centric point of view.
Going Further Back into Maize's History
As we previously found that the modern industrial breeding altered maize's relationship with the N-cycling microbiome it host's in the rhizosphere. We were interested in taking a step further back to see how maize's wild progenitor, teosinte, differs in microbial recruitment to the rhizosphere. The results from this study suggest that domestication and breeding has resulted in altered interaction with the N-cycling microbiome. These wild N-cycling microbiome traits are interesting as they may have the potential to be incorporated into modern breeding programs to improve sustainability.
