An evolutionarily ancient fatty acid desaturase is required for the synthesis of hexadecatrienoic acid, which is the main source of the bioactive jasmonate in Marchantia polymorpha

Abstract

Jasmonates are fatty acid-derived hormones that regulate multiple aspects of plant development, growth and stress responses. Bioactive jasmonates, defined as the ligands of the conserved COI1 receptor, differ between vascular plants and bryophytes (jasmonoyl-L-isoleucine (JA-Ile) and dinor-12-oxo-10,15(Z)-phytodienoic acid (dn-OPDA), respectively). The biosynthetic pathways of JA-Ile in the model vascular plant Arabidopsis thaliana have been elucidated. However, the details of dn-OPDA biosynthesis in bryophytes are still unclear.Here, we identify an orthologue of Arabidopsis fatty-acid-desaturase 5 (AtFAD5) in the model liverwort Marchantia polymorpha and show that FAD5 function is ancient and conserved between species separated by more than 450 million years (Myr) of independent evolution. Similar to AtFAD5, MpFAD5 is required for the synthesis of 7Z-hexadecenoic acid. Consequently, in Mpfad5 mutants, the hexadecanoid pathway is blocked, dn-OPDA concentrations are almost completely depleted and normal chloroplast development is impaired.Our results demonstrate that the main source of wounding-induced dn-OPDA in Marchantia is the hexadecanoid pathway and the contribution of the octadecanoid pathway (i.e. from OPDA) is minimal.Remarkably, despite extremely low concentrations of dn-OPDA, MpCOI1-mediated responses to wounding and insect feeding can still be activated in Mpfad5, suggesting that dn-OPDA may not be the only bioactive jasmonate and COI1 ligand in Marchantia.

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

“…Four Dirigent-like protein genes belong to the wound-inducible and MpERF15-dependent gene cluster (Mp DIR17 , Mp DIR38 , Mp DIR42 , and Mp DIR43 ). Among these, Mp DIR38 (Mp5g16520) has been identified before as a wound-inducible marker ( 27 , 29 , 35 ) and was confirmed by RT-qPCR to be MpERF15 dependent (fig. S3C).…”

Volatile chemical composition of Octoblepharum albidum Hedw. (Bryophyta) from the Brazilian Amazon

“…Hexadecanoic acid can be converted into unsaturated fatty acid, possibly contributing, at least partially, to the synthesis of longer fatty acids, such as eicosapentaenoic acid, which can deter herbivory [ 20 ]. Eicosapentaenoic acid (C20) and arachidonic acid (C20) are produced in high concentrations by bryophytes, but are rarely found in other plant groups [ 21 ].…”

Genome-Wide Identification and Expression Analysis of Fatty Acid Desaturase (FAD) Genes in Camelina sativa (L.) Crantz

“…The intracellular pathway of fatty acid desaturation is generally regulated by FADs (fatty acid desaturases) in plants, including Camelina [ 9 , 12 , 15 , 16 , 17 , 18 ]. Desaturase activity in fatty acid biosynthesis was originally discovered in the cytoplasm of the different tissues of the plant [ 19 ].…”

“…In addition, the acetylation of the histones of FAD3 also affects fatty acid biosynthesis in seeds [ 25 ]. FAD5 is required for hexadecenoic acid (C16:3) synthesis in the chloroplasts of Marchantia polymorpha [ 15 ]. Notably, FAD5 regulates autoimmunity in plant cells by catalyzing palmitate acid [ 12 ].…”