IDBELLA, MOHAMED (2022) Negative plant-soil feedback in agroecosystems and natural plant communities: the role of soil chemistry, microbiota, and self-DNA. [Tesi di dottorato]

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As plants grow, they alter their soil environment, including nutrient availability and soil biota. These effects can affect seedling survival and growth as part of a process called plant-soil feedback (PSF), thus altering plant population and community dynamics. Negative PSF is defined as the rise of negative conditions for plant vegetative and reproductive performance introduced into the soil by the plant itself. This phenomenon is known in agronomy as "soil fatigue". This Ph.D. thesis aims to increase the knowledge of PSF processes in both agricultural and natural ecosystems. Specific objectives were investigated in the following chapters. In the first chapter, we investigated the phytotoxicity dynamics of litter decomposition of different plant species on the growth of Trifolium repens and Triticum durum. We then evaluated the impact of seed-associated endophytic fungi on the target species to different litter species with variable chemical properties. The hypothesis tested was that fungal endophytes would increase plant resistance to inhibitory effects of litter, based on their known beneficial effects on host plants. In the second chapter, knowing that simultaneous colonization of a common host plant by endophytes and arbuscular mycorrhizal fungi (AMF) can affect not only the plant itself but also the next generation of the host plant via changes in the soil through PSF processes, we investigated whether the interaction between fungal and bacterial endophytes in seeds and AMF affects the next generation of plants. Fungal seed endophytes have been reported to induce NPSF, and their association with AMF has been described as antagonistic. Therefore, we hypothesized that such association would increase the intensity of NPSF due to the reported antagonism on the host. However, we hypothesized that the association of bacterial endophytes in the seed with AMF would produce a positive PSF because each of these microbes has been shown to have multiple benefits for the host plant. In the third chapter, on the other hand, before investigating the effect of the soil microbial community, including soil-borne pathogens and mutualists, on the generation of NPSF, we wanted to provide evidence that each plant species produces a specific microbial fingerprint under its canopy due to its specific litter decomposition and root exudates in the soil. Our hypothesis is that the chemistry of litter varies from plant to plant, resulting in a specific microbial fingerprint. It is hypothesized that this specific effect is due to the specific chemical properties of the shrubs' litter as it falls and decomposes, in addition to the plants' root exudates, resulting in different changes in soil chemistry and microbial composition. Therefore, the objective of this chapter was to provide basic information and novel insights into the environmental selection of soil microbial communities by each of the most abundant species-specific plants in a Mediterranean ecosystem. In the fourth chapter, we observed an NPSF result in the field in the form of a Janzen-Connell (JC) distribution pattern. Our initial field observations suggested that Euphorbia dendroides, a deciduous shrub, has a recruitment pattern consistent with JC distribution in a Mediterranean shrub area in southern Italy (Cape of Palinuro). For this reason, we first quantified whether JC distribution recruitment effectively occurs. In addition, because Euphorbia coexists with five woody species, we quantified recruitment under heterospecific shrubs as well. We then investigated the ecological causes of the observed pattern. Specifically, we investigated whether soil chemistry and/or soil microbiota explained the observed pattern of seedling recruitment. We also explored differences in microclimate among shrub species by monitoring air temperature and light availability at different times of the year. We expected Euphorbia recruitment density to be positively correlated with soil fertility, light, temperature buffer effect, and beneficial soil microbes, while negatively correlated with soilborne pathogens. Furthermore, in the fifth chapter, we transferred the challenge this time from natural to agricultural ecosystems. Specifically, we examined how eight crops promote or inhibit conspecific and heterospecific growth through changes in the soil. The exclusivity of the work is because we used a large number of plants with a high combination number during the second round of growth, i.e., the reaction phase. More importantly, we used the entire soil history for the response phase and not just 10% conditioned soil inoculum as most studies did. We assumed that plant communities in the conditioning phase would influence soil chemical properties and soil biotic composition, and we expected that soil biota would influence the establishment of future plant communities in the response phase. Therefore, the objective of this chapter was to test the effects of the different soil legacies established by each plant species during the conditioning phase on the chemical and microbial properties of the soil and, consequently, on the growth of conspecifics and heterospecifics during the response phase. Finally in the sixth chapter, we conditioned Arabidopsis thaliana over a long period to affect soil biotic and abiotic properties through both root exudates and litter decomposition. After the conditioning phase, the plants were removed and the soil was subjected to four different treatments, namely sterilization by autoclaving, washing with tap water, addition of 10% activated carbon and untreated control. Then, another growth cycle was started. After the response phase, the plant biomass grown in each of the four treatments was recorded, as well as the soil chemical properties and microbiota, using Shotgun sequencing. In addition, for the first time, we quantified A. thaliana self-DNA in each of the treated soils as well as in the preconditioned soil using chloroplast rbcL DNA primers. The purpose of this study was to detect the accumulation of self-DNA in the soil during the conditioning phase and to show that this exDNA is associated with the increase in NPSF. In addition, we wanted to test whether soil sterilization leads to confounding in clarifying the mechanisms behind the NPSF, as this treatment affects both soil microbial communities, particularly soil pathogens, and soil exDNA. Furthermore, we wanted to test the theory that activated carbon accumulates exDNA in the soil, thus amplifying the effects of the NPSF.

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