Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme

Abstract

Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA). In the presence of JA-Ile, the COI1 receptor physically interacts with JAZ repressors, leading to their degradation, resulting in the transcription of JA-responsive genes by MYC transcription factors. Although the biosynthesis of JA-Ile is conserved in vascular plants, it is not recognized by COI1 in bryophytes and is not biologically active. In the liverwort Marchantia polymorpha, dinor-OPDA (dn-OPDA), a homolog of OPDA with two fewer carbons, and its isomer dn-iso-OPDA accumulate after wounding and are recognized by COI1 to activate downstream signaling. The moss Calohypnum plumiforme produces the antimicrobial-specialized metabolites, momilactones. It has been reported that JA and JA-Ile are not detected in C. plumiforme and that OPDA, but not JA, can induce momilactone accumulation and the expression of these biosynthetic genes, suggesting that OPDA or its derivative is a biologically active molecule in C. plumiforme that induces chemical defense. In the present study, we investigated the biological functions of OPDA and its derivatives in C. plumiforme. Searching for the components potentially involving oxylipin signaling from transcriptomic and genomic data revealed that two COI1, three JAZ, and two MYC genes were present. Quantification analyses revealed that OPDA and its isomer iso-OPDA accumulated in larger amounts than dn-OPDA and dn-iso-OPDA after wounding. Moreover, exogenously applied OPDA, dn-OPDA, or dn-iso-OPDA induced the transcription of JAZ genes. These results imply that OPDA, dn-OPDA, and/or their isomers potentially act as biologically active molecules to induce the signaling downstream of COI1-JAZ. Furthermore, co-immunoprecipitation analysis showed the physical interaction between JAZs and MYCs, indicating the functional conservation of JAZs in C. plumiforme with other plants. These results suggest that COI1-JAZ-MYC mediated signaling is conserved and functional in C. plumiforme.

Widely Targeted Metabolomics Reveals the Effects of Soil on the Metabolites in Dioscorea opposita Thunb.

“…The amino acids and derivatives jasmonoyl-L-isoleucine, L-valyl-L-leucine, and L-cysteine were upregulated (with 26.92-, 2.96-, and 1422.22-fold increments, respectively); while 6-hydroxydopaquinone, γ-glutamyl-L-valine, and 5-oxoproline were downregulated (with 0.46-, 0.00-, and 0.48-fold decrements, respectively) in LCY relative to SCY. Jasmonoyl-L-isoleucine [ 30 ] and L-cysteine [ 31 ] are important active metabolites that regulate defense responses to various abiotic stress and developmental processes in plants. L-cysteine treatment is a safe and promising method to control postharvest brown rot, due to the activation of defense-related responses of the fruits to infection, and has a protective effect on postharvest fruits [ 31 ].…”

Insights into the Jasmonate Signaling in Basal Land Plant Revealed by the Multi-Omics Analysis of an Antarctic Moss Pohlia nutans Treated with OPDA

“…OPDA is more than just a jasmonate precursor and has been demonstrated to exert both COI1-independent and COI1-dependent biological activities [ 2 , 32 ]. In addition, exogenous application of OPDA, dn-OPDA, or dn- iso -OPDA induces the transcription of JAZ transcripts in bryophytes [ 17 , 22 , 23 ]. OPDA, dn-OPDA, and their isomers function as forceful signal molecules to induce the signaling downstream of COI1-JAZ in bryophytes [ 17 , 22 ].…”

“…In addition, exogenous application of OPDA, dn-OPDA, or dn- iso -OPDA induces the transcription of JAZ transcripts in bryophytes [ 17 , 22 , 23 ]. OPDA, dn-OPDA, and their isomers function as forceful signal molecules to induce the signaling downstream of COI1-JAZ in bryophytes [ 17 , 22 ]. Particularly, lots of genes and pathways are preferentially induced by OPDA or Ile-conjugate of OPDA (OPDA–Ile) in a COI1-independent manner [ 33 ].…”

“…The moss Physcomitrium patens and liverwort Marchantia polymorpha can synthesize OPDA but lack OPR3 (OPDA reductase) that catalyzes the hormone product of JA–lle in vascular plants [ 11 , 16 ]. The COI1 receptor is functionally conserved in land plants but the ligands it binds are dn- cis -OPDA and dn- iso -OPDA in M. polymorpha and Calohypnum plumiforme [ 16 , 17 ]. However, the signal transduction and the endogenous responses involved in OPDA signaling remain elusive in bryophytes [ 18 ].…”

Organelles and phytohormones: a network of interactions in plant stress responses

“…OPDA is found in marine algae, terrestrial algae, mosses, and ferns, but the full jasmonate synthesis pathway is absent in these organisms. Recent work suggested that dnOPDA is the evolutionary precursor of JA-Ile and can interact with the COI receptor orthologs of mosses ( Monte et al 2018 ; Inagaki et al , 2021 ). These findings indicate that the origin of jasmonate signaling can be directly connected to the chloroplast.…”