Inhibitory and toxic effects of extracellular self‐DNA in litter: a mechanism for negative plant–soil feedbacks?

Abstract

SummaryPlant-soil negative feedback (NF) is recognized as an important factor affecting plant communities. The objectives of this work were to assess the effects of litter phytotoxicity and autotoxicity on root proliferation, and to test the hypothesis that DNA is a driver of litter autotoxicity and plant-soil NF.The inhibitory effect of decomposed litter was studied in different bioassays. Litter biochemical changes were evaluated with nuclear magnetic resonance (NMR) spectroscopy. DNA accumulation in litter and soil was measured and DNA toxicity was assessed in laboratory experiments.Undecomposed litter caused nonspecific inhibition of root growth, while autotoxicity was produced by aged litter. The addition of activated carbon (AC) removed phytotoxicity, but was ineffective against autotoxicity. Phytotoxicity was related to known labile allelopathic compounds. Restricted 13 C NMR signals related to nucleic acids were the only ones negatively correlated with root growth on conspecific substrates. DNA accumulation was observed in both litter decomposition and soil history experiments. Extracted total DNA showed evident species-specific toxicity.Results indicate a general occurrence of litter autotoxicity related to the exposure to fragmented self-DNA. The evidence also suggests the involvement of accumulated extracellular DNA in plant-soil NF. Further studies are needed to further investigate this unexpected function of extracellular DNA at the ecosystem level and related cellular and molecular mechanisms.

Inhibitory effects of extracellular self‐DNA: a general biological process?

“…The recent observations by Mazzoleni et al (2015) of inhibitory effects by extracellular self-DNA in plants provided new perspectives for understanding litter autotoxicity and negative plant-soil feedbacks. The authors reported significant evidence that fragmented extracellular DNA (exDNA) has a concentration dependent and species-specific inhibitory effect on the growth of plants.…”

Does a plant detect its neighbor if it is kin or stranger? Evidence from a common garden experiment

“…A novel evidence proposed by Mazzoleni and his co-authors showed that extracellular self-DNA appears to possess a range of unique signaling properties that could explain the mechanism of regulation of species coexistence and competition (Mazzoleni et al 2015a,b, Cartenì et al 2016). As we k��� t�at DNA a�t� a� a� i��ivi��al���e�i�� ���e���i�t, as well as it is exudated into the soil and persists for a long time.…”

Spatial analysis of phylogenetic community structure: New version of a classical method

“…In this framework, Mazzoleni et al (2015a) investigated the autotoxic effect of decomposed litter of twenty plant species from Mediterranean and temperate environments on root proliferation in different bioassays. Their results indicate a general occurrence of litter autotoxicity related to the exposure to fragmented extracellular DNA.…”

“…In this view, the spatial aggregation of conspecifics induced by local dispersal needs to be disrupted to some extent by mechanisms increasing within-species segregation, like distance-or density-dependent mortality (Chesson 2000). Such inverse relationship between local conspecific density and individual performance has been related to the activity of host-specific insects or fungi (Janzen 1970, Connell 1971, the build-up of negative plant-soil feedback due to the accumulation of species-specific soil-borne pathogens Clay 2000, van der Putten et al 1993), the changing composition of soil microbial communities (Bever 1994, Klironomos 2002, or the release of autotoxic compounds from decaying litter (Singh et al 1999, Mazzoleni et al 2015a, 2015b. All these mechanisms, which are linked to the physical and chemical properties of plants rather than to their functional characters, will locally increase species diversity by reducing the chance of conspecific juveniles to colonize sites close to adult individuals.…”