Have we unknowingly altered the maize microbiome interaction?

Maize germplasm chronosequence shows crop breeding history impacts recruitment of the rhizosphere microbiome

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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.

Maize (Zea mays L.), colloquially known as corn, has experienced intense human-driven selection since its domestication in Mexico 9000 years ago. For the past 70 years of this history, modern industrial agriculture (i.e., advanced crop breeding and high nutrient inputs) has provided maize with a new suite of environmental challenges to face. Knowing this historical context infused with our relatively recent understanding of plant microbiomes, we were interested in whether this modern anthropogenic selection may have inadvertently altered functional microbial community associations in the plant rhizosphere. 

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 (Fig. 1).

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Once we had the necessary germplasm for our chronosequence, we decided to examine how these plants altered a standardized microbial community under controlled greenhouse conditions with identical starting soil inoculum (Image.1). Plant rhizospheres were harvested and we sequenced 16S rRNA genes and fungal ITS regions, and quantified microbial genes involved in nitrogen cycling.

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.

If you’re interested in the plant microbiome and agricultural  sustainability, please check out the full paper (“Maize germplasm chronosequence shows crop breeding history impacts recruitment of the rhizosphere microbiome”) is available at ISMEj: https://www.nature.com/articles/s41396-021-00923-z 

Alonso Favela

Ph.D. Candidate , University of Illinois at Urbana-Champaign