The Trichoderma fungal species and the bacteria Bacillus species were described as inducers of plant systemic resistance in relation to their antagonistic activity. The objective of this study was to evaluate the effect of selected strains of Bacillus amyloliquefaciens (I3) and Trichoderma harzianum (A) on inducing systemic resistance in Arabidopsis thaliana as a model for plant molecular genetics. The microorganisms were identified and were confirmed for their antagonistic potential in vitro and in vivo in previous studies. In order to explore this mechanism, two mutants of A. thaliana carrying a PR1 promoter (a conventional marker of salicylic acid (SA) pathway) and LOX2 promoter (a marker triggering jasmonic acid (JA) pathway activation) were analyzed after inoculating antagonists. Transgenic reporter line analysis demonstrated that B. amyloliquefaciens I3 and T. harzianum A induce A. thaliana defense pathways by activating SA and JA at a high level compared to lines treated with chemical elicitors of references (acibenzolar-S-methyl (Bion 50 WG (water-dispersible granule)), SA, and methyl jasmonate). The efficacy of B. amyloliquefaciens I3 and T. harzianum A in inducing the defense mechanism in A. thaliana was demonstrated in this study.

The transmission of seed-borne pathogens by the germinating seed is responsible for major crop diseases. The immune responses of the seed facing biotic invaders are poorly documented so far. The Arabidopsis thaliana/Alternaria brassicicola patho-system was used to describe at the transcription level the responses of germinating seeds and young seedling stages to infection by the necrotrophic fungus. RNA-seq analyses of healthy versus inoculated seeds at 3 days after sowing (DAS), stage of radicle emergence, and at 6 and 10 DAS, two stages of seedling establishment, identified thousands of differentially expressed genes by Alternaria infection. Response to hypoxia, ethylene and indole pathways were found to be induced by Alternaria in the germinating seeds. However, surprisingly, the defense responses, namely the salicylic acid (SA) pathway, the response to reactive oxygen species (ROS), the endoplasmic reticulum-associated protein degradation (ERAD) and programmed cell death, were found to be strongly induced only during the latter post-germination stages. We propose that this non-canonical immune response in early germinating seeds compared to early seedling establishment was potentially due to the seed-to-seedling transition phase. Phenotypic analyses of about 14 mutants altered in the main defense pathways illustrated these specific defense responses. The unexpected germination deficiency and insensitivity to Alternaria in the glucosinolate deficient mutants allow hypothesis of a trade-off between seed germination, necrosis induction and Alternaria transmission to the seedling. The imbalance of the SA and jasmonic acid (JA) pathways to the detriment of the JA also illustrated a non-canonical immune response at the first stages of the seedling.

Seeds play a vital role in the perpetuation of plant species, both in natural environments and agriculture. However, they often face challenges from biotic stresses, such as seed-borne pathogenic fungi. The transgenerational transmission of these seed-borne fungi, along with their dissemination during seed commercialization, can contribute to the emergence of global epidemic diseases, resulting in substantial economic losses. Despite the recognized impact of seed-borne pathogens on agriculture, our understanding of seed–pathogen interactions remains limited. This review establishes parallels between the current state of knowledge regarding seed responses to pathogen interactions and well-established plant defense models, primarily derived from typical physiological conditions observed during leaf infections. Examining fragmented results from various pathosystems, this review seeks to offer a comprehensive overview of our current understanding of interactions during seed development and germination. The necrotrophic interactions in Brassicaceae are described using recent transcriptomic and genetic studies focused on the Arabidopsis/Alternaria pathosystem, which illustrates original response pathways in germinating seeds that markedly differ from the general concept of plant–pathogen interactions. The co-existence of regulatory mechanisms affecting both seed resistance and susceptibility, potentially promoting fungal colonization, is examined. The vulnerable response during germination emerges as a crucial consideration in the context of sustainable plant health management in agriculture.

Little is known about the effect of nitrogen nutrition on seedling susceptibility to seed-borne pathogens. We have previously shown that seedlings grown under high nitrate (5 mM) conditions are less susceptible than those grown under low nitrate (0.1 mM) and ammonium (5 mM) in the Arabidopsis-Alternaria brassicicola pathosystem. However, it is not known how seedling metabolism is modulated by nitrogen nutrition, nor what is its response to pathogen infection. Here, we addressed this question using the same pathosystem and nutritive conditions, examining germination kinetics, seedling development, but also shoot ion contents, metabolome, and selected gene expression. Nitrogen nutrition clearly altered the seedling metabolome. A similar metabolomic profile was observed in inoculated seedlings grown at high nitrate levels and in not inoculated-seedlings. High nitrate levels also led to specific gene expression patterns (e.g., polyamine metabolism), while other genes responded to inoculation regardless of nitrogen supply conditions. Furthermore, the metabolites best correlated with high disease symptoms were coumarate, tyrosine, hemicellulose sugars, and polyamines, and those associated with low symptoms were organic acids (tricarboxylic acid pathway, glycerate, shikimate), sugars derivatives and β-alanine. Overall, our results suggest that the beneficial effect of high nitrate nutrition on seedling susceptibility is likely due to nutritive and signaling mechanisms affecting developmental plant processes detrimental to the pathogen. In particular, it may be due to a constitutively high tryptophan metabolism, as well as down regulation of oxidative stress caused by polyamine catabolism.

Little is known about the effect of nitrogen nutrition on seedling susceptibility to seed-borne pathogens. We have previously shown that seedlings grown under high nitrate (5 mM) conditions are less susceptible than those grown under low nitrate (0.1 mM) and ammonium (5 mM) in the Arabidopsis-Alternaria brassicicola pathosystem. However, it is not known how seedling metabolism is modulated by nitrogen nutrition, nor what is its response to pathogen infection. Here, we addressed this question using the same pathosystem and nutritive conditions, examining germination kinetics, seedling development, but also shoot ion contents, metabolome and selected gene expression. Nitrogen nutrition clearly altered the seedling metabolome. A similar metabolomic profile was observed in inoculated seedlings grown at high nitrate levels and in not inoculated-seedlings. High nitrate levels also led to specific gene expression patterns (e.g. polyamine metabolism), while other genes responded to inoculation regardless of nitrogen supply conditions. Furthermore, the metabolites best correlated with high disease symptoms were coumarate, tyrosine, hemicellulose sugars and polyamines, and those associated with low symptoms were organic acids (tricarboxylic acid pathway, glycerate, shikimate), sugars derivatives and β-alanine. Overall, our results suggest that the beneficial effect of high nitrate nutrition on seedling susceptibility is likely due to nutritive and signaling mechanisms affecting developmental plant processes detrimental to the pathogen. In particular, it may be due to a constitutively high tryptophan metabolism, as well as down regulation of oxidative stress caused by polyamine catabolism.

Seeds play a vital role in the perpetuation of plant species, both in natural environments and agriculture. However, they often face challenges from biotic stresses, such as seedborne pathogenic fungi. The transgenerational transmission of these seedborne fungi, along with their dissemination during seed commercialization, can contribute to the emergence of global epidemic diseases, resulting in substantial economic losses. One such pathogenic fungus is Alternaria brassicicola, responsible for causing black spot disease in Brassicaceae. This necrotrophic seedborne fungus negatively impacts plant development, consequently affecting crop production and seed quality. To gain a deeper understanding of the interaction between seeds and necrotrophic fungi, the Arabidopsis thaliana/Alternaria brassicicola model pathosystem has been extensively studied. Recent transcriptomic and genetic studies revealed a distinctive immune response of seeds against this pathogen, divergent from the immune response described in the plant vegetative phase. In germinating seeds and seedlings, the necrotrophic fungus seems to induce susceptible response [1]. It was observed at the RNA level that to the detriment of jasmonic acid pathway, Alternaria induced the salicylic acid and glucosinolate (GSL) pathways. Genetic evidence identified that seedling necrosis, potentially beneficial to the growth of the necrotrophic agent, is hypersensitive response mediated by GSL pathway. Transmission of necrotrophic fungal from seed to seedling unveils novel regulations of the immune response, that would illustrate a trade-off between seedling establishment and fungal infection. This knowledge is promising to sustainably ensure the sanitary quality of crops.