Host plasticity and the microbiome underlie acquired salt tolerance in a freshwater plant

Background/Question/Methods

When faced with rapid environmental changes, species will also have to respond rapidly in order to persist. Evolutionary genetic changes in DNA sequence are not the only way species may respond. A plethora of plastic mechanisms may allow species to respond even in the absence of beneficial genetic variation, and can occur within a single individual, or across generations as transgenerational effects. Microbiomes are also affected by stresses, either directly by the stressor or indirectly via host changes, and ecological or evolutionary change in microbiomes might contribute to environmental responses of their hosts. One major source of novel stress is the expansion of the urban environment. For example, urban aquatic organisms face increasingly salty conditions, as high road salt use drives up salinity in urban runoff and even groundwater. Duckweed (Lemna minor) is a tiny floating freshwater plant that persists across extreme rural to urban ecotones, including salty ponds. By manipulating the presence and absence of the microbiome, and interfering with a normal transgenerational plasticity mechanism, we quantified the contribution of plastic changes within duckweed, as well as changes in its associated microbiome that allow duckweed to persist in salty conditions along the urban-to-rural ecotone.

Results/Conclusions

Lines of duckweed from more urban sites tolerated higher levels of salt than duckweeds collected from rural areas with low road densities. However, this depended on both microbiomes and normal DNA cytosine methylation, a process that can regulate gene expression. We found that without the differences conferred by microbiomes and DNA cytosine methylation, salt tolerance among lines was similar. We also documented that acute salt stress can plastically increase the tolerance of even relatively salt tolerant urban duckweeds over only a few generations in clonal lines. This acute salt-tolerance trades off with growth in salt-free conditions, and occurred regardless of microbiome presence or interference with normal DNA cytosine methylation. Acquired acute salt tolerance was affected, but not increased by the presence of the microbiome, and so appears to be driven by a mechanism internal to duckweed other than DNA methylation, such as direct passing of RNA transcripts or other molecules during clonal offspring formation.