Jasmonates: News on Occurrence, Biosynthesis, Metabolism and Action of an Ancient Group of Signaling Compounds

Abstract

: Jasmonic acid (JA) and its related derivatives are ubiquitously occurring compounds of land plants acting in numerous stress responses and development. Recent studies on evolution of JA and other oxylipins indicated conserved biosynthesis. JA formation is initiated by oxygenation of α-linolenic acid (α-LeA, 18:3) or 16:3 fatty acid of chloroplast membranes leading to 12-oxo-phytodienoic acid (OPDA) as intermediate compound, but in Marchantiapolymorpha and Physcomitrellapatens, OPDA and some of its derivatives are final products active in a conserved signaling pathway. JA formation and its metabolic conversion take place in chloroplasts, peroxisomes and cytosol, respectively. Metabolites of JA are formed in 12 different pathways leading to active, inactive and partially active compounds. The isoleucine conjugate of JA (JA-Ile) is the ligand of the receptor component COI1 in vascular plants, whereas in the bryophyte M. polymorpha COI1 perceives an OPDA derivative indicating its functionally conserved activity. JA-induced gene expressions in the numerous biotic and abiotic stress responses and development are initiated in a well-studied complex regulation by homeostasis of transcription factors functioning as repressors and activators.

Keywords: JA biosynthetic enzymes; JA bypass; JA signaling; Jasmonic acid (JA) metabolites; active JA compounds; occurrence; transcription factors.

Figure 1

Scheme on Jasmonic Acid/Jasmonic Acid Isoleucine Conjugate (JA/JA-Ile) biosynthesis and action in four different compartments of a plant cell. Upon release of α-linolenic acid by the A₁-type lipases (PLIP, Plastid Lipase; PLA₁, Phospholipase A1 of flowers) from galactolipids, cis-(+)-12-Oxophytodienoic Acid (cis-(+)-OPDA) is formed in plastids by a 13-LOX, AOS and AOC. Following transport into peroxisomes, OPDA is reduced by OPDA reductase3 (OPR3) und undergoes ß-oxidation of the carboxylic acid side chain to JA (shown as the initially formed right configuration (+)-7-iso-JA). Upon release into the cytosol, JA is conjugated with amino acids by JAR1 or exported by a JA-transporter JAT1. The same transporter allows import of JA-Ile into the nucleus, where JA-Ile perception and JA-Il-induced gene expression takes place (for details and references cf. Part 3). Mutants known for Arabidopsis (red) or tomato (green) are indicated.

Figure 2

The bypath in JA biosynthesis. OPDA and dnOPDA are formed in chloroplasts and converted to JA and 4,5-ddh-JA, respectively, in peroxisomes. In opr3-3 plants, peroxisomal OPDA is metabolized to dinor-OPDA (dnOPDA), tetranor-OPDA (tnOPDA) and 4,5-didehydro-JA (4,5-ddh-JA), which is reduced to JA by OPR2 after release into the cytosol. Black arrows show the canonical pathway, red arrows highlight the new pathway identified in opr3-3 plants. Red parallel lines indicate block in the conversion of OPDA and dnOPDA within the opr3-3 mutant. The newly identified property of OPR2 in opr3-3 is marked in red (redrawn based on Reference [102] with permission).

Figure 3

Structures of Arabidopside A, B, C, and D.

Figure 4

Metabolism of JA. Methylation to JA-methyl ester, JA glucosyl ester formation, decarboxylation to cis-jasmone, hydroxylation to 12-hydroxyJA, sulfation of 12-hydroxyJA, O-glucosylation of 12-hydroxyJA to 12-O-glucosyl-JA, conjugation of JA with amino acids, preferentially isoleucine to give JA-Ile, methylation to JA-Ile methyl ester, 12-hydroxylation of JA-Ile, carboxylation of 12-OH-JA-Ile, O-glucosylation of JA-Ile to 12-O-glucosyl-JA-Ile, and formation of JA-Ile glucosyl ester are indicated. Known involved enzymes are JAO2, jasmonic acid oxidase2, JOX1,2,3,4, jasmonate induced oxidase 1,2,3,4, JAR1, jasmonoyl-isoleucine synthetase, JA-Ile-12-hydroxylase CYP94B3, 12-OH-JA-Ile carboxylase CYP94C1, amidohydrolases IAR3 and ILL6, JMT, JA methyl transferase, ST2a, 12-OH-JA sulfotransferase. The lactone of 12-OH-JA-Ile was added even though detection for plants is missing so far. Biologically inactive compounds are outlined with solid lines (▬▬▬), partially active compounds are outlined with dashed and dotted lines (▬ ^.▬ ^.▬) and active compounds are outlined with dotted lines (-----), the biological activity of 12-carboxy-JA, as well as of JA-Ile-glucosyl ester and JA-Ile methyl ester are unknown (modified after Reference [132] with permission).

Figure 5

A simplified model of JA-Ile perception and signaling via the SCF^COI1-JAZ co-receptor complex. At low level of JA-Ile, the JAZ repressors recruit the co-repressor complex consisting of NINJA, TOPLESS (TPL) and the histone deacetylase (HDA), interact with and repress positive regulators of JA signaling such as the transcription activator MYC2, and also inhibits negative regulators of JA signaling such as the transcriptional repressors IIId bHLH factors. Upon external stimuli or developmental changes levels of JA-Ile are elevated leading to perception of JA-Ile by the COI1-JAZ co-receptor and degradation of JAZs via the 26S proteasome. The downstream transcription factors are activated to regulate synergistically or antagonistically expression of JA-responsive genes and JA responses. MYC2 associates with the MED25 subunit of the mediator complex, binds to the G-box motif of the target promoters and activates JA-responsive genes. The IIId bHLH factors antagonize MYC2 via competitive binding to the G-box motif and inhibiting JA-responsive genes. COI1, ASK2, CULLIN1, Rbx and E2 are components of the SCF^COI1 complex. Ub, ubiquitin. Modified with permission from Reference [3] (color in print).