Soil sickness and negative plant-soil feedback: A reappraisal of hypotheses

Soil sickness (SS) is the rise of negative conditions for plant vegetative and reproductive performances induced into the soil by the plant itself. In natural ecosystems, plant ecologists refer to SS as negative plant-soil feedback (NPSF). Scope of this review is to provide an updated picture of the current SS understanding by an explicit comparison between agro-ecosystems and natural plant communities. By an extensive analysis of literature we found that SS is pervasive in agro-ecosystems, occurring in 111 cultivated plants belonging to 41 taxonomic families. Concerning NPSF in natural plant communities, we found evidence of this phenomenon for a total of 411 vascular plants belonging to 72 plant families. NPSF occurs in most of the terrestrial ecosystems, including tropical and temperate forests, coastal sand dunes, old fields and grassland, deserts, as well as heathland and tundra. Three main hypotheses have been proposed to explain SS: (i) soil nutrient depletion or imbalance; (ii) buildup of soilborne pathogen and parasite populations, coupled with a shift in soil microbial community composition; (iii) release of phytotoxic and autotoxic compounds during decomposition of crop residues. Evidences from both agroecosystems and natural plant communities undoubtedly ruled out the nutrient deficiency as a primary causal factor. Moreover, the massive use of mineral fertilizers, especially under intensive cultivation systems, appears an incorrect strategy that only exacerbates the decline of soil quality by inducing acidification and salinization. Soilborne pathogens are often isolated from symptomatic plants and many autotoxic compounds have been identified and quantified from sick soil. However, both the pathogenic and autotoxicity hypotheses are still unable to fully explain the species-specificity, as well as the long durability of SS observed in field conditions. The recent discovery that extracellular DNA (exDNA) has self-inhibitory effects, support the autotoxicity hypothesis, nevertheless this is a totally new topic, and more solid and systematic field investigations are needed. A better understanding of the causes of SS is a necessary step to develop eco-friendly solutions to overcome this problem.