The role of extracellular self-DNA in plant-soil negative feedback and autotoxicity

Background/Question/Methods

Plant-soil feedback is considered an important factor shaping plant community structure and diversity. Theoretical modelling work demonstrated that the build-up of plant-soil negative feedback could explain both gradients of species diversity and spatial organization of vegetation. In this context, autotoxicity has been proposed as a possible mechanism of such negative feedback, relating it to the release of inhibitors by litter decomposition and their removal dynamics by water.
In this study we tested the hypothesis that litter autotoxicity could be due to extracellular DNA. This theory, advanced on the basis of theoretical reasoning, was thoroughly investigated by integrating ecological, phytochemical, and biomolecular studies. Specifically, a throughput metabolomic characterization by nuclear magnetic resonance (¹³C NMR) was performed on a large set of plant litter materials at different decomposition stages. Finally, we tested the effect of purified DNA on a range of organisms from microbes to higher plants.

Results/Conclusions

Results indicated a general occurrence of species-specific litter toxicity. We found that extracellular self-DNA accumulates in litter during decomposition, with strong relationship between this process and root growth inhibition. This discovery reveals a new unexpected function of DNA at ecosystem level. Moreover, tests using purified extracellular self-DNA demonstrated the general occurrence of inhibition in plants and various organisms including bacteria, fungi, algae, protozoa, and insects. Such findings provide strong evidence for DNA involvement in autotoxicity. Further studies are needed to assess the relative importance of this process compared with complementary theories on plant-soil negative feedback and the potential role of extracellular self-DNA in self-recognition.