Transcriptional profiling reveals conserved and species-specific plant defense responses during the interaction of the early divergent plantPhyscomitrium patenswithBotrytis cinerea

Abstract

Bryophytes were among the first plants that colonized earth and they evolved key defense mechanisms to counteract microbial pathogens present in the new environment. Although great advances have been made on pathogen perception and subsequent defense activation in angiosperms, limited information is available in early divergent land plants. In this study, a transcriptomic approach uncovered the molecular mechanisms underlying the defense response of the bryophyte Physcomitrium patens against the important plant pathogen Botrytis cinerea. A total of 3.072 differentially expressed genes were significantly affected during B. cinerea infection, including genes encoding proteins with known function in angiosperm immunity and involved in pathogen perception, signaling, transcription, hormonal signaling, metabolic pathways such as shikimate and phenylpropanoid, and proteins with diverse role in defense against biotic stress. Similarly as in other plants, B. cinerea infection leads to downregulation of genes involved in photosynthesis and cell cycle progression. These results highlight the existence of evolutionary conserved defense responses to pathogens throughout the green plant lineage, suggesting that they were probably present in the common ancestors of land plants. Moreover, several genes acquired by horizontal transfer from prokaryotes and fungi, and a high number of P. patens-specific orphan genes were differentially expressed during B. cinerea infection, indicating that they are part of the moss immune response and probably played an ancestral role related to effective adaptation mechanisms to cope with pathogen invasion during the conquest of land.

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

“…Several secreted enzymes of B. cinerea are recognized by plant leucine-rich repeat receptors, including PGs [ 93 ], and BcXYG1 [ 42 ], leading to activation of plant defense. Interestingly, P. patens induces rapidly the expression levels of a high number of genes encoding these type of receptors during B. cinerea infection [ 28 ]. However, further research is needed to understand if some of these receptors recognize PGs and other fungal PAMPs in moss tissues.…”

“…However, further research is needed to understand if some of these receptors recognize PGs and other fungal PAMPs in moss tissues. Moreover, we observed that two genes encoding putative plant pectin methyl-esterase inhibitor were upregulated in P. patens after B. cinerea colonization [ 28 ]. These inhibitors could be involved in making the wall more resistant to degradation by fungal enzymes by increasing methylated pectin in the cell wall [ 94 ].…”

“…However, the activation of these defense mechanisms is not sufficient to stop B. cinerea growth and colonization, leading to plant decay. Recently, we have shown that P. patens responds to this fungal pathogen with transcriptional reprogramming of 3072 plant genes, which encode proteins involved in pathogen perception, signaling, transcription, hormonal signaling, secondary metabolic pathways and proteins with diverse role in defense against biotic stress [ 28 ]. To gain more insights into B. cinerea infection and virulence strategies displayed during moss colonization, we focused on the transcriptional response of B. cinerea genes during the infection process of P. patens .…”

An ancient route towards salicylic acid and its implications for the perpetualTrichormus–Azollasymbiosis

“…Weisshaar and Jenkins 1998, Deluc et al 2006, Xie et al 2008). PAL genes are responsive to biotic stressors (Oliva et al 2015, Reboledo et al 2021). It is therefore, in general, not surprising that genes from the phenylpropanoid pathway are responsive to the treatment.…”