The Role of Seed Endophytes in the Drought Tolerance of the Xerophytic Invasive Plant Lactuca serriola

Abstract

In nature, plants form holobionts with a wide array of microbes, among which seed endophytes transmitted vertically to offspring emerge as crucial partners, particularly for invasive plants colonizing new habitats. These seed endophytes exhibit diverse plant growth-promoting traits that aid in plant establishment and growth across various environments, including drought conditions. Notably, drought-tolerant bacteria capable of producing specific material exopolysaccharides play a pivotal role in enhancing the soil water preservation and promoting plant growth under drought stress. However, the effectiveness of these plant growth-promoting bacteria often varies depending on the host species or genotype. Given its xerophytic nature and propensity for wind dispersal in arid seasons, the invasive alien plant Lactuca serriola would be thought to benefit from drought-tolerant seed endophytes, potentially bolstering its resilience to drought stress. Therefore, investigating the interaction between drought-tolerant seed endophytes and L. serriola promises to yield valuable insights into the role of seed endophytes in the invasiveness and adaptive mechanisms of invasive plants. This study aims to identify and characterize drought stress-alleviating seed endophytes from wild L. serriola and elucidate the underlying mechanisms. To achieve this goal, seed endophytes were isolated and identified, and drought-tolerant EPS-producing bacteria were selected using in vitro assays. Subsequently, the stress-alleviating effects of selected isolates were examined across various plant species, including Arabidopsis thaliana, Lactuca serriola, Lactuca sativa, Zea mays, and Camelina sativa. Furthermore, the study investigated genotype-specific responses by assessing five different L. serriola. The potential causes of host-specificity were explored, focusing on plant root exudate components. Finally, the stress-alleviating mechanisms of isolates was elucidated through transcriptome analysis. The results of this study revealed that out of 128 bacterial seed endophytes isolated from wild L. serriola, 42 representative strains exhibited at least one plant growth-promoting trait and drought tolerance. Among these, 12 isolates were selected for in planta assays based on their performance under drought conditions. Notably, Kosakonia cowanii GG1 demonstrated significant improvements in soil water contents and shoot growth under stress compared to uninfected control plants, suggesting the potential of seed endophytes as a novel strategy for invasive plants to thrive in challenging environments. Moreover, the study found that the infection of seed endophytes yielded different outcomes in various plant species. While several isolates positively impacted the plant and soil characteristics of L. serriola under drought, the effects varied depending on the L. serriola genotype. Pearson’s correlation coefficients indicated that rhiozosheath formation played the crucial role in the stress-alleviating effect of isolates. However, the isolates positively affected A. thaliana or L. serriola did not exhibit any stress-alleviating effect on three model plants. Analysis of organic acids within the root exudate revealed qualitative differences among plant species, suggesting their involvement in host-specific interactions. Additionally, K. cowanii GG1 and Erwinia tasmaniensis YJ6, which were effective in L. serriola P2 demonstrated differential responses to organic acid components. These results imply the importance of host species in plant-bacteria interaction and suggest that the root exudate would be a possible factor involved in host-specificity. Finally, the study unveiled that E. tasmaniensis YJ6 primed the L. serriola P2 for drought resistance under benign water conditions. The infected plants exhibited induced signal pathway of the stress-related hormone abscisic acid and accumulated osmoprotectants before the onset of stress, suggesting the potential of E. tasmaniensis YJ6 for biological priming against drought stress. In conclusion, this thesis underscores the pivotal role of seed endophytes in the adaptive mechanisms of L. serriola against drought stress. It highlights the significance of host-specific interactions and biological priming mechanisms in understanding plant-bacteria interactions in the context of environmental stress.