Seed Transmission of Pathogens: Non-Canonical Immune Response in Arabidopsis Germinating Seeds Compared to Early Seedlings against the Necrotrophic Fungus Alternaria brassicicola

Abstract

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.

A novel “ceasefire” model to explain efficient seed transmission ofXanthomonas citripv.fuscansto common bean

“…Recent data from the compatible interaction Alternaria brassicicola-A. thaliana , used as seed transmission model, showed that host defense pathways are subjected to drastic changes during the germination process (Ortega-Cuadros et al, 2022). It would be interesting to explore whether such rearrangements take place in other compatible interactions such as Xcf -bean and if a link with epigenetic modifications exists.…”

First Report on the Seed Immune Response to Fungal Necrotrophs Attack

“…However, the immune responses of seeds to biotic interactions during germination have been little studied, although this step is crucial to control seed-borne pathogen transmission to the new plant [21,24]. The model pathosystem Arabidopsis thaliana/Alternaria brassicicola has been recently used to describe gene regulation induced by the necrotrophic interaction during germination and seedling establishment [1,21,61].…”

“…They involve different physical barriers such as cell wall appositions, hormonal signaling and antimicrobial metabolites such as phytoalexins or reactive oxygen species (ROS) and proteins [13,14,19,20] (Figure 1b). Recent studies using the pathosystem Arabidopsis thaliana/Alternaria brassicicola [21] have described non-canonical defense responses in the germinating seeds 1 compared to the established model describing defense mechanism against a necrotrophic agent [20,22], most of which are based on the physiological model of rosette leaf inoculation [23]. This review addresses the specific features of germinating seeds in terms of their responses to necrotrophic attacks [1].…”

“…Recent studies using the pathosystem Arabidopsis thaliana/Alternaria brassicicola [21] have described non-canonical defense responses in the germinating seeds 1 compared to the established model describing defense mechanism against a necrotrophic agent [20,22], most of which are based on the physiological model of rosette leaf inoculation [23]. This review addresses the specific features of germinating seeds in terms of their responses to necrotrophic attacks [1]. This new knowledge will be placed in the context of general concepts on plant resistance mechanisms to biotic aggression and the particularities of necrotrophic interaction that is documented by the Arabidopsis thaliana/Alternaria brassicicola pathosystem.…”

“…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.…”