Occurrence of jasmonates during cystocarp development in the red alga Grateloupia imbricata

Abstract

In this study, we highlight the effects of methyl jasmonate (MeJa) on cystocarp development in the red macroscopic alga Grateloupia imbricata. In G. imbricata, jasmonate release is related to the reproductive state, as fertile thalli (i.e., those that have cystocarps) released significant amounts of this volatile compound (1.27 ± 0.20 mM · mg fw · h ) compared with infertile thalli (0.95 ± 0.12 mM · mg fw · h ). Treating G. imbricata thalli with MeJa revealed a significant increase in cystocarp number (1.5 ± 0.27 cystocarps · mm ), which was ~7.5-fold greater than in untreated thalli (0.2 ± 0.07 cystocarps · mm ). Maturation was completed within 48 h with MeJa treatment, a shortening of the typical >3-week maturation period, and included the opening of cystocarps and the presence of dehiscent cavities. Release rates of jasmonates after exogenous MeJa treatment were also modified based on the cystocarp maturation level. All of these effects were reduced in the presence of phenidone, which blocks MeJa production, indicating that the MeJa action is genuine. The effects of MeJa during cystocarp maturation were not replicated by derivatives of reactive oxygen species from the same jasmonic acid biosynthetic pathway, as the activities of scavenger enzymes and lipid peroxidation were unchanged between infertile and fertile thalli. Therefore, a reactive oxygen species-based mechanism is not involved during cystocarp development. We conclude that MeJa has an independent function as a growth regulator during G. imbricata reproduction.

Analysis of the Transcriptome of the Red Seaweed Grateloupia imbricata with Emphasis on Reproductive Potential

“…Studies of in vitro carposporogenesis in G. imbricata have demonstrated that polyamines, ethylene, and methyl jasmonate act as elicitors of cystocarp development, spore release, and the timing of the development of reproductive structures; moreover, knowledge of the functional mechanisms of these elicitors has informed the search for candidate genes that govern reproduction in red algae [5,8,9,12]. Therefore, in our transcriptome analysis, we selected transcripts related to polyamine metabolism such as ornithine decarboxylase (ODC), SAMS, SAM decarboxylase, copper amine oxidase, spermidine/spermine synthase, putrescine aminopropyltransferase, agmatine deimidase, and N-carbamoylputrescine amidohydrolase (supplementary file 2).…”

“…Methyl jasmonate induces both cystocarp maturation and sporulation [5]. In higher plants, jasmonic acid is synthesized by the oxygenation of linolenic acid via lipoxygenase, and a methyl group is then added to jasmonic acid, which yields methyl jasmonate; however, in seaweeds which perceive and respond to methyl jasmonate, the relevant biosynthetic enzymes have not been characterized.…”

“…Because genomic information concerning the genes involved in jasmonates biosynthesis is limited in seaweeds, our study will help researchers carry out analyses of the expression and function of these genes and take advantage of insights on alga reproduction. It is also worth stressing that although the role of jasmonates and the involvement of reactive oxygen species in G. imbricata reproduction were recently described [5], hitherto the genes have not been annotated for algae. Figure 4A shows the genes involved in jasmonic acid-responsive pathways, which presumably occur in seaweeds.…”

“…Culture of G. imbricata in glycerol-containing media can increase polymer biosynthesis [3,4], and this seaweed responds to growth regulators as elicitors of carposporogenesis and sporulation [4,5,6,7,8,9]. The focus of research with this seaweed species has since transitioned from growth performance to the identification of gene-encoding proteins responsible for the synthesis of polymers and the small molecules ethylene, methyl jasmonate, and polyamines as the main elicitors of cystocarp maturation and spore release [10,11,12].…”

Insight into the Mechanism of Red Alga Reproduction. What Else Is Beyond Cystocarps Development?

“…Changes related to the maturing of thalli are favoured by volatile growth regulators, which also lead to both cystocarps dehiscence with a marked reduction of the maturity period, and the presence of different reproductive structures in the same individual [5]. Moreover, other evidence such as sudden losses of seaweed mats and alternating life cycles could also give cues on how volatile compounds act as a signal to trigger the reproductive process.…”