XAP5 CIRCADIAN TIMEKEEPER Affects Both DNA Damage Responses and Immune Signaling in Arabidopsis

Abstract

Numerous links have been reported between immune response and DNA damage repair pathways in both plants and animals but the precise nature of the relationship between these fundamental processes is not entirely clear. Here, we report that XAP5 CIRCADIAN TIMEKEEPER (XCT), a protein highly conserved across eukaryotes, acts as a negative regulator of immunity in Arabidopsis thaliana and plays a positive role in responses to DNA damaging radiation. We find xct mutants have enhanced resistance to infection by a virulent bacterial pathogen, Pseudomonas syringae pv. tomato DC3000, and are hyper-responsive to the defense-activating hormone salicylic acid (SA) when compared to wild-type. Unlike most mutants with constitutive effector-triggered immunity (ETI), xct plants do not have increased levels of SA and retain enhanced immunity at elevated temperatures. Genetic analysis indicates XCT acts independently of NONEXPRESSOR OF PATHOGENESIS RELATED GENES1 (NPR1), which encodes a known SA receptor. Since DNA damage has been reported to potentiate immune responses, we next investigated the DNA damage response in our mutants. We found xct seedlings to be hypersensitive to UV-C and γ radiation and deficient in phosphorylation of the histone variant H2A.X, one of the earliest known responses to DNA damage. These data demonstrate that loss of XCT causes a defect in an early step of the DNA damage response pathway. Together, our data suggest that alterations in DNA damage response pathways may underlie the enhanced immunity seen in xct mutants.

ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response

“…In some cases, seemingly incongruent findings could reflect species-specific differences ( 159 ), mutants that generate changes in the phenotypic resistance levels via changes in the sensitivity to a certain signal rather than signal intensity ( 160 ), the context-dependent action of alternative mechanisms, e.g., during different parts of the cell cycle ( 79 ), different times of the day or different contributions of partly redundant elements. For example, plants possess two pathways for the synthesis of SA, the isochorismate-pathway in which ISOCHORISMATE SYNTHASE (ICS) catalyses the synthesis of the central precursor molecule and the PHENYLALANINE AMMONIA LYASE (PAL) pathway in which PAL, the first enzyme in phenylpropanoid synthesis, converts phenylalanine to trans-cinnamic acid ( 77 ).…”

XAP5 CIRCADIAN TIMEKEEPERregulates RNA splicing and the circadian clock via genetically separable pathways

“…A recent study showed that the NTC-associated protein MOS4-ASSOCIATED COMPLEX SUBUNIT 5A (MAC5A) physically interacts with the 26S proteasome and regulates its activities in response to DNA damage (Meng et al, 2022). Intriguingly, we recently reported that loss of XCT function also disturbs the DNA damage response pathway (Kumimoto et al, 2021). Thus, it is possible that XCT works with PRP19 in this pathway separately from its role in RNA processing.…”

“…Fission yeast and Chlamydomonas XAP5 proteins associate with chromatin and directly regulate transcription (Anver et al, 2014; Li et al, 2018). In addition to its role in the clock, Arabidopsis XCT has been implicated in diverse processes including small RNA production, immune signaling, and DNA damage responses (Fang et al, 2015; Xu et al, 2017; Kumimoto et al, 2021). Notably, NTC components have also been reported to function in all these pathways (Jia et al, 2017; Maréchal et al, 2014; Chanarat and Sträßer, 2013).…”