The multifactorial basis for plant health promotion by plant-associated bacteria

Abstract

On plants, microbial populations interact with each other and their host through the actions of secreted metabolites. However, the combined action of diverse organisms and their different metabolites on plant health has yet to be fully appreciated. Here, the multifactorial nature of these interactions, at the organismal and molecular level, leading to the biological control of plant diseases is reviewed. To do so, we describe in detail the ecological significance of three different classes of secondary metabolites and discuss how they might contribute to biological control. Specifically, the roles of auxin, acetoin, and phenazines are considered, because they represent very different but important types of secondary metabolites. We also describe how studies of the global regulation of bacterial secondary metabolism have led to the discovery of new genes and phenotypes related to plant health promotion. In conclusion, we describe three avenues for future research that will help to integrate these complex and diverse observations into a more coherent synthesis of bacterially mediated biocontrol of plant diseases.

FIG. 1.

The multifactorial nature of biological control of plant diseases. (1) Cellular expression of biocontrol-related genes and secretion of bioactive metabolites. Production of bioactive metabolites occurs within the complex network of cellular metabolism, which is influenced by internal regulons as well as external signals. The diversity of these genes, metabolites, and networks has not been fully elucidated. (2) Distribution and dynamics of plant-associated microbial populations with biocontrol capacities. Subsets of these populations may act to alter plant health status across a complex mosaic of aggregates and biofilms found on all host tissues. Such assemblages may contain biocontrol (beige ovals) and/or pathogenic bacteria (yellow ovals), but the distribution, diversity, and dynamics of such populations are not fully characterized. (3) Host responses to microbial activities integrated through the symplast at the cell, organ, and whole-plant levels. The stimulus from multiple contact points between plant hosts and diverse microbial epiphytes and endophytes certainly occurs and can affect the partitioning of nutrients and the development of phenotypes indicating plant health status. However, how such multiple signals are processed and integrated locally and systemically remains a mystery.