Plant extracellular self-DNA inhibits growth and induces immunity via the jasmonate signaling pathway

Abstract

Plants have evolved sophisticated mechanisms to detect various forms of danger. Damage-associated molecular patterns (DAMPs) are endogenous danger molecules that are released from damaged cells and activate the innate immunity. Recent evidence suggests that plant extracellular self-DNA (esDNA) can serve as a DAMP molecule. However, the mechanisms by which esDNA functions are largely unknown. In this study, we confirmed that esDNA inhibits root growth and triggers reactive oxygen species (ROS) production in a concentration- and species-specific manner in Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum L.). Furthermore, by combining RNA sequencing, hormone measurement and genetic analysis, we found that esDNA-mediated growth inhibition and ROS production are achieved through the jasmonic acid (JA) signaling pathway. Specifically, esDNA induces JA production and the expression of JA responsive genes. The esDNA-mediated growth inhibition, ROS production and gene expression are impaired in the JA-related mutants. Finally, we found that the JA signaling pathway is required for the esDNA-elicited resistance against the pathogens Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000. This finding highlights the importance of JA signaling in esDNA-mediated biological effects, thereby providing insight into how esDNA functions as a DAMP.

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

“…The levels of JA peaked at 30 min and those of SA at 24 h ( Figure 2 ; Supplementary Figure S3 ). Subsequent treatments revealed self/nonself-specific effects of DNA on H 2 O 2 and both hormones and in all cases, strongest effects were triggered by self-DNA ( Figure 2 ), similar to earlier observations, although with minor differences between species ( 20 – 22 , 26 , 35 , 36 ). The response times and levels reached by the three signals fall clearly within the standard kinetics of the three signals ( 119 – 121 ).…”

“…Strikingly, stronger responses to self- in comparison to nonself-DNA were reported in most, although not all, of the studies that compared DNA from different sources. Even the ‘Mazzoleni-effect’ – a dosage-dependent inhibition of growth by self-DNA, but not nonself-DNA that has been described originally by the group of Stefano Mazzoleni – could subsequently be confirmed in different models, including a tree ( Alnus glutinosa ), freshwater and marine algae and the nematode, Caenorhabditis elegans ( 18 , 21 , 22 , 30 , 31 , 35 , 37 , 38 ). Differential responses to self- versus nonself-DNA are significant even when nonself-DNA from closely related genotypes (species of the same genus or ecotypes of the same species) is used ( 21 , 26 , 31 , 35 , 36 , 38 ).…”

“…Treatments with plant DNA, genomic or plasmid bacterial DNA, or synthetic single stranded oligodeoxynucleotides (ssODNs), were shown to trigger early immune responses that are highly conserved between plants and mammals, including Ca 2+ fluxes, membrane depolarization, the formation of reactive oxygen species (ROS) such as hydrogen peroxide (H 2 O 2 ), or the activation of mitogen-activated protein kinases (MAPKs) ( 9 , 20 – 22 , 25 , 27 , 34 , 35 ). The responses include massive transcriptomic reprogramming ( 24 , 25 , 35 ), and studies at the phenotypic level reported not only increased immunity (‘resistance’) to microbial pathogens, but also increased ‘defence’ to plant-specific pests such as leaf and sap-sucking herbivores ( 21 , 23 , 26 , 27 , 29 , 33 – 36 ). Strikingly, stronger responses to self- in comparison to nonself-DNA were reported in most, although not all, of the studies that compared DNA from different sources.…”

“…However, on the one hand, an induction by DNA has been reported for traits that are typically controlled via WR as well as SAR. Further, more recent support for the PTI model comes from a study that linked resistance-induction by self-DNA in peach ( Prunus persica ) fruits to the brassinosteroid insensitive 1-associated receptor kinase 1 (BAK1) – a cytoplasmatic co-receptor that interacts with various PRRs of DAMPs and PAMPs ( 34 ) - and from two studies that reported self-DNA-induced JA-synthesis in A. thaliana and common bean ( Phaseolus vulgaris ) ( 35 , 36 ). On the other hand, self-/nonself specific effects are mainly reported for early, not enemy-specific immune signals which have also been reported for the DDR, and as far as we know, no PRRs that could act as dsDNA receptors have been reported for plants or could be predicted by in silico approaches ( 4 , 63 – 65 ).…”

The intrinsically disordered C‐terminus of purinoceptor P2K1 fine‐tunes plant responses to extracellular ATP

“…Extracellular ATP (eATP) has been shown to play multiple roles in plant growth and development, including root growth and stress responses [6,18,20,40,41]. It has been reported that eATP suppresses growth and alters the growth orientation of the root and hypocotyl of Arabidopsis by affecting hormone signaling pathways [6,[41][42][43][44]. Some reports suggest that the P2K1 receptor is partially involved in eATP-mediated plant growth [44].…”