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The wound activated ERF15 transcription factor drives Marchantia polymorpha regeneration by activating an oxylipin biosynthesis feedback loop

ABSTRACT: The regenerative potential in response to wounding varies largely along species. Within the plant lineage, the liverwort Marchantia polymorpha displays an extraordinary regeneration capacity. However, its molecular pathways controlling the initial regeneration response post wounding is currently unknown. In Arabidopsis, the transcription factor ETHYLENE RESPONSE FACTOR 109 (ERF109) plays an essential role in tissue regeneration. Here, we demonstrate that the Marchantia MpERF15 transcription factor gene represents a functional ortholog of ERF109, being instantly activated following wounding and being essential for gemmaling regeneration following tissue incision. MpERF15 is a downstream target of the MpCOI1 oxylipin receptor, but differently from Arabidopsis ERF109 its wound responsiveness is COI1 independent. At the other hand, and again differently from ERF109, MpERF15 drives oxylipin biosynthesis by controlling the upstream MpAOS2 and MpAOC biosynthesis genes. The resulting rise in the oxylipin dnOPDA levels results in an increase in gemma cell number and apical notch organogenesis, giving rise to highly disorganized and compact thalli. Our data pinpoint MpERF15 as a key factor activating an oxylipin biosynthesis amplification loop following wounding that eventually results in re-activation of cell division and regeneration, and suggest that the genetic networks controlling oxylipin biosynthesis in response to wounding might have been reshuffled over evolution.

ORGANISM(S): Marchantia polymorpha

PROVIDER: GSE196912 | GEO | 2022/02/19

REPOSITORIES: GEO

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Project description:The allene oxide synthase (AOS) branch and the hydroperoxide lyase (HPL) branch of the oxylipin pathway function in plant responses to diverse stresses and have potential cross-talks between each other in the biosynthesis and signaling regulation, but there is still an absence of direct evidence and detailed information about this communication. Here, we identified and characterized a jasmonates acid (JA) overproduction mutant, cea62, by screening the Constitutive Expression of AOS gene (cea) from rice T-DNA insertion mutant library. Map-based cloning was used to isolate the target gene as the hydroperoxide lyase OsHPL3 gene. The gene expression, HPL enzyme activity and its resulting products, (E)-2-hexenal, were all depleted in the cea62 mutant, which resulted in dramatic JA overproduction and activation of JA signaling in the mutant. Consistent with the formation of the lesion mimic phenotype and the timing of the induction for some defense responsive genes, the activation of JA biosynthesis and signaling was regulated in a developmental way, just as the way by which OsHPL3 was regulated in the wild type plant. Microarray data showed that the JA-governed defense response was greatly activated in the cea62 mutant plant and the cea62 plant obtained enhanced resistance to the bacterial blight pathogen Xanthomonasoryzaepvoryzae (Xoo) T1 strain. Wounding response was attenuated in the cea62 mutant at an early developmental stage, while it was partially recovered when JA levels were elevated at a later developmental stage in the cea62 mutant. But, the wounding response was not altered at different developmental stages in the wild type plant. These findings suggest that these two branches of the oxylipin pathways crosstalked in the biosynthesis and signaling pathways and cooperated with each other to function in diverse stress responses. We compared the gene expression profile in leaf tissues of the wild-type plant and the cea62 mutant after lesion mimic phenotype appeared two months after sowing. Total RNAs were extracted from leaf blades from the rice (Oryza sativa L.) wild-type Nipponbare plant and from leaf blades of the rice (Oryza sativa L.) cea62 mutant in the Nipponbare (ssp japonica) background at two months after sowing. Three replicates of the cea62 mutant and wild type were performed.

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The wound activated ERF15 transcription factor drives Marchantia polymorpha regeneration by activating an oxylipin biosynthesis feedback loop

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