Plant evolution driven by interactions with symbiotic and pathogenic microbes

Abstract

During 450 million years of diversification on land, plants and microbes have evolved together. This is reflected in today’s continuum of associations, ranging from parasitism to mutualism. Through phylogenetics, cell biology, and reverse genetics extending beyond flowering plants into bryophytes, scientists have started to unravel the genetic basis and evolutionary trajectories of plant-microbe associations. Protection against pathogens and support of beneficial, symbiotic, microorganisms are sustained by a blend of conserved and clade-specific plant mechanisms evolving at different speeds. We propose that symbiosis consistently emerges from the co-option of protection mechanisms and general cell biology principles. Exploring and harnessing the diversity of molecular mechanisms used in nonflowering plant-microbe interactions may extend the possibilities for engineering symbiosis-competent and pathogen-resilient crops.

Plant immune system activation is necessary for efficient interaction with auxin secreting beneficial bacteria

“…A prevalent view of mutualistic interactions is that symbiosis evolved through exploitative interactions that became attenuated over evolutionary time 55–57 . Parallels were found between the immune system signaling pathway and the symbiotic association between plants and specialized mutualists, like the interaction between legumes and rhizobia 55, 58 as well as the association between plants and arbuscular mycorrhizal fungi 59 .…”

The Coevolution of Plants and Microbes Underpins Sustainable Agriculture

“…Interestingly, because Rubisco is a large protein and is in high concentrations in plant leaves, it is the most abundant protein in leaves [ 45 ] and the most abundant protein globally [ 46 ]; it is a critical source of protein for herbivores and, interestingly, has an exceptionally good amino acid balance for herbivores [ 47 ]; through the efficiencies of having an amino acid profile matching the protein source microbes (cyanobacteria), by becoming plant Rubisco-chloroplasts, probably influenced/drove the amino acid composition of herbivorous animals. Additionally, in extreme environmental condition or under situations of limited resource supplement, plant survival also depends on the microbes to obtain what they need through building and maintain key symbiotic relationships and managing pathogenic ones [ 48 ].…”

“…In fact, microbial members of the rhizomicrobiome are increasingly recognized for their beneficial impacts on plant systems, with the understanding that we have only scratched the surface of both their diversity and roles in development. During the course of evolution, plants have evolved strategies to exchange chemical signals with microbes which confers the ability to (1) protect against pathogen attacks, (2) take advantage of functions provided by beneficial microbes (ranging from nutrient acquisition to immune system activation), and (3) recruit anti-pathogen microbes [ 48 ]. As we argued in a previous paper [ 11 ], plants are best conceptualized as holobionts, which takes into account the phytomicrobiome and organelles (mitochondria and chloroplasts; entrained microbes) that are essential to plant survival [ 84 ].…”

“…Only a limited number of phytomicrobiome interactions have been studied in depth, to characterize symbiotic relationships in only a few land plant lineages; the results of these studies indicate that there are a wide range of these relationships that have not yet been characterized. In addition, plant evolution was also driven by interactions with parasitic and pathogenic microbes [ 48 ]. Even when the rigidly symbiotic legume-rhizobia and plant-mycorrhizal fungi relationships are excluded, the large and coordinated phytomicrobiome population is indispensable to plant growth.…”

Will Plant Genome Editing Play a Decisive Role in “Quantum-Leap” Improvements in Crop Yield to Feed an Increasing Global Human Population?

“…However, few plant–microbe interactions have been studied in depth, with only a few land plant lineages. Subsequent investigations may reveal new types of symbiotic or pathogenic interactions [ 117 , 122 ]. Synthetic biology tools may provide an opportunity to design plant–microbe associations that improve crop productivity.…”