Harnessing Population Genomics to Understand How Bacterial Pathogens Emerge, Adapt to Crop Hosts, and Disseminate

Abstract

Crop diseases emerge without warning. In many cases, diseases cross borders, or even oceans, before plant pathologists have time to identify and characterize the causative agents. Genome sequencing, in combination with intensive sampling of pathogen populations and application of population genetic tools, is now providing the means to unravel how bacterial crop pathogens emerge from environmental reservoirs, how they evolve and adapt to crops, and what international and intercontinental routes they follow during dissemination. Here, we introduce the field of population genomics and review the population genomics research of bacterial plant pathogens over the past 10 years. We highlight the potential of population genomics for investigating plant pathogens, using examples of population genomics studies of human pathogens. We also describe the complementary nature of the fields of population genomics and molecular plant-microbe interactions and propose how to translate new insights into improved disease prevention and control.

Understanding Plant Immunity as a Surveillance System to Detect Invasion

“…Many of them display variation within a single species, or a relatively limited taxonomic distribution, suggestive of recent evolution. This, coupled with data suggesting the existence of independently evolved receptors for different domains of flagellin and EF-Tu, highlights the dynamic nature and distribution of PRRs and that PRR evolution is similar to the evolution of R genes responding to host-specific pathogens (26,101,148).…”

“…These include the suppositions that PRRs are old and more slowly evolving than R genes and are therefore more highly conserved, and that MAMPs are stable and broadly detected while effectors are variable and detected by specific hosts. However, a number of examples from well-studied systems do not support these assumptions but instead suggest that plant receptors are evolving to accurately detect invasion and, conversely, invader patterns are under pressure to avoid recognition (101,148). This is regardless of their MTI-ETI classification.…”

“…Whereas it is generally stated that MTI is more durable and ETI is ephemeral, clear exceptions in agricultural settings have been noted (15,68,99) and the idea that PRRs will generically result in durable resistance can be questioned (26,148). This, coupled with the omission of DAMPs, results in the limited predictive framework of the zigzag model to address durable disease resistance.…”

Best Practices for Population Genetic Analyses

“…First, coalescent analyses provide powerful tools that go beyond the scope of this review yet provide complementary approaches to those discussed here Carbone and Kohn 2001;Drummond et al 2005;Goss 2015;Goss et al 2009a;Grünwald and Goss 2011;Hudson 1990). Second, the field of population genetics is now increasingly relying on high throughput sequencing technologies to genotype individuals at thousands of SNPs using for example GBS or RADseq (Andrews and Luikart 2014;Davey et al 2011;Elshire et al 2011;Grünwald et al 2016b;Luikart et al 2003;Vinatzer et al 2014;Weigel and Nordborg 2015). With GBS, scientists must rethink their toolbox given a range of new challenges such as removal of linked SNPs, massive amounts of missing data, imputation, ensuring appropriate allele calls, and use of reference genomes among others (Grünwald et al 2016b).…”

Population Genomics of Fungal and Oomycete Pathogens

“…For example, such studies have led to a greater realization of the importance of horizontal gene transfer (HGT) and interspecific hybridizations in pathogen origins. HGT of pathogenicity gene clusters has featured prominently in the evolution of bacterial pathogens (100), but more recently HGT has also been well documented in fungi and oomycetes (35, 38, 77). All told, these types of population genetics studies have the potential to provide a deeper and finer-grained understanding of the biology, genetics, and evolution of plant pathogens.…”