PAMP-triggered genetic reprogramming involves widespread alternative transcription initiation and an immediate transcription factor wave

Abstract

Immune responses triggered by pathogen-associated molecular patterns (PAMPs) are key to pathogen defense, but drivers and stabilizers of the growth-to-defense genetic reprogramming remain incompletely understood in plants. Here, we report a time-course study of the establishment of PAMP-triggered immunity (PTI) using cap analysis of gene expression (CAGE). We show that around 15% of all transcription start sites (TSSs) rapidly induced during PTI define alternative transcription initiation events. From these, we identify clear examples of regulatory TSS change via alternative inclusion of target peptides or domains in encoded proteins, or of upstream open reading frames (uORFs) in mRNA leader sequences. We also find that 60% of PAMP-response genes respond earlier than previously thought. In particular, a cluster of rapidly and transiently PAMP-induced genes is enriched in transcription factors whose functions, previously associated with biological processes as diverse as abiotic stress adaptation and stem cell activity, appear to converge on growth restriction. Furthermore, examples of known potentiators of PTI, in one case under direct MAP kinase control, support the notion that the rapidly induced transcription factors could constitute direct links to PTI signaling pathways and drive gene expression changes underlying establishment of the immune state.

The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and 5’ transcript length determination in Arabidopsis

“…Thus, the new TSSs used in the plant BAF-like mutants most likely correspond to previously found TSSs that are not preferentially used in unchallenged conditions but might be chosen in certain developmental or environmental situations. Importantly, changes in TSS selection have been reported in different tissues or upon environmental changes (87,(89)(90)(91). The extended 5´ transcript regions observed in the tpf and minu mutants could influence mRNA function through, for example, the incorporation of upstream ORFs and localisation signals that can impact translation efficiency and final localisation of proteins, respectively (87,89).…”

Ralstonia solanacearum effector RipAK suppresses homodimerization of the host transcription factor ERF098 to enhance susceptibility and the sensitivity of pepper plants to dehydration

“…Plants possess sophisticated defense machinery to fend off the invasion of pathogens. For example, plants perceive PAMPs to activate PTI and cause a series of rapid immune responses, including the accumulation of phytohormones SA and JA, burst of ROS, and the activation of mitogen-activated protein kinase, as well as the transcriptional reprogramming of the genes related to defense (Li et al, 2015(Li et al, , 2016Thieffry et al, 2022). Thus, this immune network prevents pathogens from successfully evading the plant defenses.…”

Transcriptional regulation of plant innate immunity

“…Alternative transcription initiation can expand the regulatory repertoire of the genome, since it may involve alternative promoters that are differentially induced upon different stimuli, or result in different transcripts and proteins ( Figure 1 I). Recently, more than 15% of the 3374 transcripts that were induced by flg22 treatment after 30 min were found to be derived from alternative transcription events [ 94 ]. The alternative transcripts for example lacked upstream open reading frames (uORFs), which may affect translation efficiency of the transcript, or their encoded proteins lacked a predicted domain or signal peptide, which could potentially alter their function.…”