The Coevolution of Plants and Microbes Underpins Sustainable Agriculture

Abstract

Terrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolved relationships with plants that range from non-dependent interactions to dependent endosymbionts. The most extreme endosymbiotic examples are the chloroplasts and mitochondria, which have become organelles and integral parts of the plant, leading to some similarity in DNA sequence between plant tissues and cyanobacteria, the prokaryotic symbiont of ancestral plants. Microbes were associated with the precursors of land plants, green algae, and helped algae transition from aquatic to terrestrial environments. In the terrestrial setting the phytomicrobiome contributes to plant growth and development by (1) establishing symbiotic relationships between plant growth-promoting microbes, including rhizobacteria and mycorrhizal fungi, (2) conferring biotic stress resistance by producing antibiotic compounds, and (3) secreting microbe-to-plant signal compounds, such as phytohormones or their analogues, that regulate aspects of plant physiology, including stress resistance. As plants have evolved, they recruited microbes to assist in the adaptation to available growing environments. Microbes serve themselves by promoting plant growth, which in turn provides microbes with nutrition (root exudates, a source of reduced carbon) and a desirable habitat (the rhizosphere or within plant tissues). The outcome of this coevolution is the diverse and metabolically rich microbial community that now exists in the rhizosphere of terrestrial plants. The holobiont, the unit made up of the phytomicrobiome and the plant host, results from this wide range of coevolved relationships. We are just beginning to appreciate the many ways in which this complex and subtle coevolution acts in agricultural systems.

Keywords: holobiont; pathogenic interaction; phytomicrobiome; plant evolution; symbiosis.

Figure 1

A range of microorganisms contribute to plant function, allowing them to become the dominant terrestrial primary producers, such as crop plants. This includes prokaryotes becoming organelles (mitochondria and chloroplasts), with cyanobacteria focused on because of their pivotal role in giving plants photosynthetic ability, through chloroplasts, and a range of other microbes forming other beneficial (plant growth promotion microbes) and negative (pathogens) associations with plants. The combination of fungi, algae (with cyanobacteria-derived chloroplasts) and, at least sometimes, cyanobacteria, resulted in a parallel “organismal” development.