Abstract
Damage-associated molecular pattern molecules (DAMPs) signal the presence of tissue damage to induce immune responses in plants and animals. Here, we report that High Mobility Group Box 3 (HMGB3) is a novel plant DAMP. Extracellular HMGB3, through receptor-like kinases BAK1 and BKK1, induced hallmark innate immune responses, including i) MAPK activation, ii) defense-related gene expression, iii) callose deposition, and iv) enhanced resistance to Botrytis cinerea. Infection by necrotrophic B. cinerea released HMGB3 into the extracellular space (apoplast). Silencing HMGBs enhanced susceptibility to B. cinerea, while HMGB3 injection into apoplast restored resistance. Like its human counterpart, HMGB3 binds salicylic acid (SA), which results in inhibition of its DAMP activity. An SA-binding site mutant of HMGB3 retained its DAMP activity, which was no longer inhibited by SA, consistent with its reduced SA-binding activity. These results provide cross-kingdom evidence that HMGB proteins function as DAMPs and that SA is their conserved inhibitor.
Highlights
As multi-cellular organisms, plants must be able to detect wounding and tissue damage, which can breach the physical barriers to pathogen infection
We recently identified human High Mobility Group Box 1 (HMGB1) as a novel Salicylic Acid-Binding Protein (SABP) and found that its Damage-associated molecular patterns (DAMPs) activities are inhibited by salicylic acid (SA) binding
We showed that i) infection by a necrotrophic pathogen releases plant HMGB3 into the apoplast, ii) extracellular, HMGB3 activates immune responses, iii) SA binds to HMGB3, and iv) this binding alters its DAMP activity
Summary
As multi-cellular organisms, plants must be able to detect wounding and tissue damage, which can breach the physical barriers to pathogen infection. Cell surface pattern-recognition receptor (PRR) complexes detect the presence of DAMPs, as well as microbe-associated molecular patterns (MAMPs), and activate a plant innate immune response termed pattern-triggered immunity (PTI) [1,3,4]. Plants lacking certain PRRs or their regulatory LRR RLKs BAK1 and BKK1 have severely compromised PTI responses. These plants fail to exhibit a rapid Ca2+ influx or an oxidative burst, and/or display reduced levels of mitogen-activated protein kinase (MAPK) activation, defense-related gene expression, and callose deposition; as a result, they exhibit decreased disease resistance
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