Toward Ecologically Relevant Genetics of Interactions Between Host Plants and Plant Growth-Promoting Bacteria

Abstract

The social movement to reduce reliance on pesticides and synthesized fertilizers and the growing global demand for sustainable food supplies require the development of eco-friendly and sustainable agricultural practices. In line, plant growth-promoting bacteria (PGPB) can participate in creating innovative agroecological systems. While the effectiveness of PGPB is highly influenced by abiotic conditions and microbe-microbe interactions, beneficial plant-PGPB interactions can also highly depend on both host and PGPB genotype. Here, the state of the art on the extent of natural genetic variation of plant-PGPB interactions and the underlying genetic architecture, in particular in Arabidopsis thaliana is reviewed. Extensive natural plant genetic variation in response to PGPB is associated with a polygenic architecture and genetic pathways rarely mentioned as being involved in the response to PGPB. To date, natural genetic variation within PGPB is little explored, which may in turn allow the identification of new genetic pathways underlying benefits to plants. Accordingly, several avenues to better understand the genomic and molecular landscape of plant-PGPB interactions are introduced. Finally, the need for establishing thorough functional studies of candidate genes underlying Quantitative Trait Loci and estimating the extent of genotype-by-genotype-by-environment interactions within the context of realistic (agro-)ecological conditions is advocated.

Keywords: GWAS; PGPB; SynCom; microbiota; natural genetic variation.

Figure 1

State of the art of the genetics of natural genetic variation of plant response to PGPB. a) Illustration of what is known about the extent of plant genetic variation in response to PGPB and the underlying genetic architecture. The interaction plot on top right illustrates the genetic variation between three plant genotypes after inoculation with a PGPB. The green, blue, and red lines correspond to a beneficial, neutral, and negative bacterial effect on genotypes G1, G2, and G3, respectively. Quantitative phenotypic variation in response to a PGPB ranging from negative to beneficial effects is represented by a gradient from red to green. Manhattan plot illustrating of polygenic architecture after performing a GWA mapping that enables a fine‐mapping of QTLs. b) Illustration of the next steps for a better understanding of the genetic and molecular mechanisms of the natural variation of plant response to PGPB. KO: knock‐out mutant line. OE: overexpressor line. Illustration of transcriptomics studies performed with an Illumina NextSeq 2000 sequencer. See text for details. Created with BioRender.com.

Figure 2

Steps for conducting a successful GWAS in a PGPB species. a) Sampling strategy to isolate genetically distinct strains of a specific PGPB species. b) Sampling root and/or leaf tissues for plating serial dilutions on media after grinding. Isolation of tens of strains of a specific PGPB species can be achieved by a community‐based culture approach c) and/or an informative‐driven approach d). e) Sequencing strategy for an accurate taxonomic affiliation and obtaining key information prior to GWA mapping. Illustration of long‐read sequencing with Nanopore PromethION 48 and a PacBio Sequel. The structural variant corresponds to a gene deletion. Created with BioRender.com.

Figure 3

Future avenues on the ecological genetics underlying natural variation of plant–PGPB interactions. a) GWAS in plants. From mono‐inoculation to microbiota: toward inoculating plants with SynComs. b) GWAS in PGPB. Considering the large fraction of private and accessory genes to run GWA mapping. c) Matrix illustrating genotype‐by‐genotype interactions between a host plant and a PGPB species. d) Effects of the inoculated plant organ and development stage on the genetics of plant–PGPB interactions. e) Effects of environmental gradients on the genetics of plant–PGPB interactions. Created with BioRender.com.