Jasmonates disrupt carrageenan synthesis during carposporogenesis in the red seaweed Grateloupia imbricata

Abstract

In this study, we monitored changes in cell wall sulfated galactans in the red seaweed Grateloupia imbricata after the rapid (48 h) induction of cystocarp maturation and carpospore development by the volatile hormone methyl jasmonate (MEJA). Synthesis of sulfated galactans, carrageenans, which requires sulfated UDP galactose, was followed by expression analysis of genes encoding phosphoglucomutase (PGM), galactose-1-phosphate uridyltransferase (GALT), and those responsible for sulfate assimilation (S-transporter and sulfate adenylyltransferase, SAT). In addition, the expression of carbohydrate sulfotransferase and galactose-6-sulfurylase responsible for the addition and removal of sulfate groups to the galactans backbone were evaluated. Structural changes, such as thallus softening, were analyzed using Fourier-transformed infrared spectroscopy (FTIR) spectra, and ploidy was assessed using flow cytometry. The results showed downregulation of most of the genes encoding precursors or those in charge of transformation into sulfated hexoses for cell wall synthesis. Furthermore, alterations in the FTIR spectrum of carrageenan from MEJA-induced fertile thalli, such as the disappearance and flattening of absorption bands, were observed. The promptness of these events and the ploidy of thalli and spores seem to confirm the induction of mitotic production of haploid spores by MEJA.

Jasmonates and Ethylene Shape Floridoside Synthesis during Carposporogenesis in the Red Seaweed Grateloupia imbricata

“…Also, it has been reported that stored polysaccharides play a role in the life cycle [ 8 ] and salinity acclimation of seaweeds [ 19 ]. Therefore, the formation and degradation of floridoside could be interwoven with sulfated polysaccharides, as carrageenan biosynthesis is also dependent on the hexose pool and reproductive stages of red seaweeds [ 3 , 4 ]. Furthermore, it is relevant that GALT expression has been associated with fluctuations in cell wall galactans in the red seaweed Gracilaria changii [ 20 ] whilst GALT expression has also accompanied cystocarp development from induced fertile thalli of G. imbricata treated with methionine ( Figure 2 ).…”

“…Furthermore, it is relevant that GALT expression has been associated with fluctuations in cell wall galactans in the red seaweed Gracilaria changii [ 20 ] whilst GALT expression has also accompanied cystocarp development from induced fertile thalli of G. imbricata treated with methionine ( Figure 2 ). Accordingly, the reduced expression of GALT , as a gene precursor of galactan synthesis, has been explained by the contribution of methionine to a pool of sulfur organic compounds in algae, which will affect the expression levels of the genes encoding proteins responsible for the conversion of glucose 6P to 1P by PGM and the transformation to UDP-galactose by GALT [ 3 , 4 ]. Thus, GALT expression is downregulated in ethylene-induced fertile thalli with cystocarps in the early development stage ( Figure 2 A), as well as when late cystocarp development stages are reached in the presence of MEJA ( Figure 2 B).…”

“…Moreover, thalli treated exogenously with plant growth volatile regulators, such as ethylene and jasmonates (MEJA), also altered gene expression of biosynthetic precursors of carrageenan synthesis, particularly the synthesis of UDP-hexoses and those in charge of adding and removing sulfated groups to/from the galactan backbone. Additionally, MEJA completely disrupted carrageenan synthesis, as FTIR spectra revealed [ 3 ]. The synthesis of carrageenan was also affected by the presence of an exogenous S-source, with implications for the assimilation and activation of the S-source [ 3 , 4 ].…”

“…Additionally, MEJA completely disrupted carrageenan synthesis, as FTIR spectra revealed [ 3 ]. The synthesis of carrageenan was also affected by the presence of an exogenous S-source, with implications for the assimilation and activation of the S-source [ 3 , 4 ].…”

“…Although the synthesis pathway of floridoside is still unconfirmed [ 9 ], it is assumed that its biosynthesis involves the transfer of a galactosyl unit from a pool of UDP- hexoses to glycerol 3-phosphate [ 10 , 11 ](G3P; Figure 1 ). In reverse, α-galactosidase cleaves galactosyl residues to form UDP-galactose units, which can be used to continue floridoside synthesis and for the synthesis of sulfated galactans [ 3 , 4 , 12 ] ( Figure 1 ). Accordingly, it was demonstrated that phosphoglucomutase ( PGM ) and galactose-1-phosphate uridyltransferase ( GALT ), encoding proteins of synthetic precursors and sustaining the pool of UDP-hexoses, altered their gene expression alongside the reproductive stages of thalli of the red seaweed Grateloupia imbricata [ 3 , 4 ].…”