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Dallery, J.-F.; Zimmer, M.; Halder, V.; Suliman, M.; Pigné, S.; Le Goff, G.; Gianniou, D. D.; Trougakos, I. P.; Ouazzani, J.; Gasperini, D.; O’Connell, R. J. Inhibition of jasmonate-mediated plant defences by the fungal metabolite higginsianin B bioRxiv (2019) DOI: 10.1101/651562
Infection of Arabidopsis thaliana by the
ascomycete fungus Colletotrichum higginsianum is characterised by an
early symptomless biotrophic phase followed by a destructive
necrotrophic phase. The fungal genome contains 77 secondary
metabolism-related biosynthetic gene clusters (BGCs), and their
expression during the infection process is tightly regulated. Deleting
CclA, a chromatin regulator involved in repression of some BGCs through
H3K4 trimethylation, allowed overproduction of 3 families of terpenoids
and isolation of 12 different molecules. These natural products were
tested in combination with methyl jasmonate (MeJA), an elicitor of
jasmonate responses, for their capacity to alter defence gene induction
in Arabidopsis. Higginsianin B inhibited MeJA-triggered expression of
the defence reporter VSP1p:GUS, suggesting it may block bioactive JA-Ile
synthesis or signalling in planta. Using the JA-Ile sensor Jas9-VENUS,
we found that higginsianin B, but not three other structurally-related
molecules, suppressed JA-Ile signalling by preventing degradation of JAZ
proteins, the repressors of JA responses. Higginsianin B likely blocks
the 26S proteasome-dependent degradation of JAZ proteins because it
inhibited chymotrypsin- and caspase-like protease activities. The
inhibition of target degradation by higginsianin B also extended to
auxin signalling, as higginsianin B treatment reduced IAA-dependent
expression of DR5p:GUS. Overall, our data indicate that specific fungal
secondary metabolites can act similarly to protein effectors to subvert
plant immune and developmental responses.