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First published online July 9, 2004; 10.1104/pp.103.037622 Plant Physiology 135:1838-1848 (2004) © 2004 American Society of Plant Biologists The Innate Immunity of a Marine Red Alga Involves Oxylipins from Both the Eicosanoid and Octadecanoid Pathways1,[w]UMR 7139 (CNRS-GOEMAR-UPMC), Station Biologique, F–29682 Roscoff cedex, France (K.B., E.G., B.K., J.-P.S., P.P.); and Laboratoire de Biochimie–EA–948, Université de Bretagne Occidentale, Faculté de Médecine, F–29285 Brest, France (F.A., E.G., J.-P.S.)
The oxygenated derivatives of fatty acids, known as oxylipins, are pivotal signaling molecules in animals and terrestrial plants. In animal systems, eicosanoids regulate cell differentiation, immune responses, and homeostasis. In contrast, terrestrial plants use derivatives of C18 and C16 fatty acids as developmental or defense hormones. Marine algae have emerged early in the evolution of eukaryotes as several distinct phyla, independent from the animal and green-plant lineages. The occurrence of oxylipins of the eicosanoid family is well documented in marine red algae, but their biological roles remain an enigma. Here we address the hypothesis that they are involved with the defense mechanisms of the red alga Chondrus crispus. By investigating its association with a green algal endophyte Acrochaete operculata, which becomes invasive in the diploid generation of this red alga, we showed that (1) when challenged by pathogen extracts, the resistant haploid phase of C. crispus produced both C20 and C18 oxylipins, (2) elicitation with pathogen extracts or methyl jasmonate activated the metabolism of C20 and C18 polyunsaturated fatty acids to generate hydroperoxides and cyclopentenones such as prostaglandins and jasmonates, and (3) C20 and C18 hydroperoxides as well as methyl jasmonate did induce shikimate dehydrogenase and Phe ammonialyase activities in C. crispus and conferred an induced resistance to the diploid phase, while inhibitors of fatty acid oxidation reduced the natural resistance of the haploid generation. The dual nature of oxylipin metabolism in this alga suggests that early eukaryotes featured both animal- (eicosanoids) and plant-like (octadecanoids) oxylipins as essential components of innate immunity mechanisms.
Signaling cascades involving compounds derived from the oxidative metabolism of polyunsaturated fatty acids (PUFAs) are known to operate in response to external stimuli in both terrestrial plants and animals. In animal systems, eicosanoids, i.e. hydroperoxides derived from C20 PUFAs, regulate cell differentiation, immune responses, and homeostasis (Funk, 2001  ). In contrast, terrestrial plants use derivatives of C18 (octadecanoids) and C16 (hexadecanoids) fatty acids as developmental or defense hormones (Weber, 2002). The biosynthesis of these so-called oxylipins involves lipoxygenases (LOXs), which are multifunctional enzymes that catalyze the oxygenation of PUFAs into hydroperoxy derivatives, then on to other secondary products (Funk, 2001; Howe and Schilmiller, 2002). In terrestrial higher plants, this leads to the synthesis of the cyclopentenone jasmonic acid (JA), a key defense hormone described in a variety of crops or cell cultures (Heitz et al., 1997; Ishiguro et al., 2001; Seo et al., 2001; Turner et al., 2002). In animals, an alternative pathway involving cyclooxygenases also leads to the synthesis of important hormones with a cyclopentenone structure, known as prostaglandins (Funk, 2001). Another pathway derived from phospholipase-released arachidonic acid, involving 5-LOX, generates other potent eicosanoid lipid mediators referred to as leukotrienes (Funk, 2001).
Marine red algae, which emerged as an independent lineage early in the evolution of eukaryotes (Baldauf et al., 2000
Altogether, marine red algae are well documented to contain a variety of oxylipins of pharmacological interest, yet nothing is known of their biological functions in the algae (Gerwick et al., 1999 Given the functions of oxylipins in animals and terrestrial plants, we addressed the hypothesis that these compounds are also involved with the innate immunity of marine red algae. We show here that, when challenged by pathogen extracts, the red alga C. crispus produces both C20 and C18 oxylipins. These are shown to arise via the activation of enzymes involved in fatty acid oxidation and induce some other defensive responses, which mediate the resistance against A. operculata invasion.
Challenge with A. operculata Elicitors Induces Release of Free Fatty Acids and Activates Oxygenation Cascades in C. crispus Gametophytes
In this plant-pathogen system, we have previously reported that C. crispus gametophytes (the resistant generation) respond to recognition of A. operculata cell-free extracts by a burst of H2O2, whereas the sporophytes (invaded by the endophyte) release only limited amounts of H2O2 (Bouarab et al., 1999
Challenge with A. operculata Elicitors Activates Oxidative Metabolism in C. crispus Gametophytes To address the potential involvement of LOXs and other fatty acid oxidases in the generation of oxidized PUFAs in C. crispus, cell-free protein extracts were incubated with various PUFAs and the generated metabolites were analyzed by LC-MS (Fig. 2). Incubation of C18:3 with protein extracts from unchallenged gametophytes resulted in the production of 13-HOTE, which accounted for the conversion of only 2.30% of the added linolenic acid substrate. In contrast, this product was detected in larger amounts after incubation of C18:3 with the protein extracts from elicited gametophytes, accounting for a conversion of 8.40% of the substrate. Low amounts of 13-hydroperoxyoctadecatrienoic acid (13-HPOTE) were also detected, representing a conversion of 0.80% of the initial substrate, likely because it might be rapidly converted into 13-HOTE and ketol derivatives (accounting for 4%). 13-HOTE was detected as only 1.40% of conversion of the substrate after incubation with extracts from elicited gametophytes which had been pretreated with n-PG. Similarly, incubation of linoleic or arachidonic acid with the protein extracts from elicited gametophytes yielded large amounts of oxylipins, mainly containing 13-hydroperoxy- and 13-hydroxyoctadecatrienoic acid [13-H(P)ODE] and 12-hydroperoxy- and 12-hydroxyeicosatetraenoic acid [12-H(P)ETE], respectively, while these compounds were not generated or were generated at very low levels only by the protein extracts from either unelicited gametophytes or elicited thalli pretreated with n-PG (data not shown).
Interestingly, in the presence of linolenic acid, both the protein fractions from control and elicited C. crispus generated a compound displaying a GC retention time (Rt; 9.5 min) and a mass spectrum (E.I. 70 eV) very similar to the fragmentation pattern of authentic methyl jasmonate (MeJA; see supplemental data, available at www.plantphysiol.org). Following incubation of protein extracts from elicited gametophytes with arachidonic acid, eluting compounds were detected with molecular masses [M-H](–) at m/z 333 and m/z 335, corresponding to the expected masses for prostaglandins. Their reverse phase (RP)-HPLC Rt and their mass fragmentation spectra were indeed very similar to those from the authentic prostaglandins B2 (PGB2, [M-H](–) m/z 333, Rt 7.3 min; Fig. 3) and B1 (PGB1, [M-H](–) m/z 335, Rt 6.1 min). Two minor products, 12-hydroxy-5,8,10,14-eicosatetraenoic (12-HETE, Rt 25.8 min) and 11,12-epoxy-5,8,14-eicosatrienoic acids (11,12-EET, Rt 37.8 min) were also characterized by their fragmentation patterns, displaying informative signals at m/z 319 (M-1), m/z 301 (M-18 loss of H2O), and by characteristic fragments due to the position of the epoxide or hydroxyl group at m/z 167 and m/z 149 for the 11,12-EET and at m/z 208 and m/z 179 for 12-HETE, similar to the mass spectra of authentic standards. In addition, LC-MS analysis revealed noncharacteristic signals at m/z 295 (M-1) and m/z 277 (M-18, loss of water), corresponding to monooxygenated linoleic acid derivatives and characteristic fragments due to the position of the epoxide group at m/z 171 and 183 for the 9,10-epoxy-12-octadecenoic acid (Rt 36.9 min) and at m/z 223 and 195 for the 12,13-epoxy-9-octadecenoic acid (Rt 34.6 min). The RP-HPLC Rts and the fragmentation patterns were very similar to those obtained with authentic standards.
The induction of an oxidative cascade was then monitored by native PAGE and in-gel detection of C18:2 peroxidation (Fig. 4A). In elicited C. crispus gametophytes, three bands with lipoxygenase or/and peroxidase activity were up-regulated, from 24 h to at least 72 h after elicitation, whereas no such activation was observed in gametophytes pretreated with n-PG or salicylhydroxamic acid (SHAM), another nonspecific inhibitor of LOXs (Macri et al., 1994 ) nor in the unchallenged gametophytes (Fig. 4A). The corresponding gel bands were excised, crushed, and incubated with linoleic or arachidonic acid, and the oxygenation products were analyzed by LC-MS (Fig. 4, B and C). Incubation of band I in the presence of linoleic acid yielded large amounts of a compound with a molecular mass [M-H](–) of 311 (Fig. 4B), which was further identified as the  - and  -ketols synthesized from 13-HPODE. Minor products, with a molecular mass [M-H](–) of 295 and showing Rts and mass spectra similar to authentic 9,10-epoxy-12-octadecenoic acid (coronaric acid) and 11,12-epoxy-9-octadecenoic acid (vernolic acid), were also generated. This band was not active in the presence of C20:4. Incubation of band II in the presence of C18:2 again yielded the - and -ketols of 13-HPODE, and it generated low amounts of oxidized compounds from C20:4 (data not shown). No product was generated at a detectable level from the incubation of band III with C18:2 and C20:4.
Methyl Jasmonate Activates Oxidative Cascades in C. crispus Gametophytes
We also investigated the effect of challenging C. crispus gametophytes with 100–µM MeJA for 6 h on their capacity to metabolize FFAs. Following the procedure described in "Materials and Methods," metabolites from both C18:2 and C20:4 were characterized from their RP-HPLC Rts and their APCI(–) mass spectra fragmentations. Incubation of protein extracts from unchallenged gametophytes in the presence of C18:2 (Fig. 5B) resulted in the production of 13-hydroxyoctadecadienoic acid (13-HODE, Rt 17.9 min), with a conversion of 4.9% of the substrate and of lower amounts of 11-hydroxyoctadecadienoic acid (11-HODE, Rt 13.3 min, 1.0%). Their fragmentation patterns displayed informative signals at m/z 295 (M-1), m/z 277 (M-18 loss of water) and characteristic fragments due to the position of the hydroxyl group respectively at m/z 195 (
Inhibitors of Fatty Acid Oxidation Reduced the Natural Resistance of C. crispus Gametophytes against A. operculata The relevance of the activation of a fatty acid oxidation pathway in the defense system of C. crispus was then further investigated in pharmacological experiments in which we tested the effects of known inhibitors of fatty acid oxidation n-PG (60 µM) or SHAM (1 mM) on the resistance of C. crispus gametophytes to infection by A. operculata zoospores. Treatments with n-PG or with SHAM did not inhibit H2O2 release following challenge of C. crispus gametophytes with A. operculata elicitor (data not shown). However, the vulnerability of C. crispus to infection was markedly increased when the gametophytic thalli were treated with the inhibitors for 20 min before inoculation with the endophyte zoospores. In control C. crispus gametophytes, infection spots were scarce at the thallus surface (frequencies of infection at the tip of 6.2 ± 0.5 spots mm–2). In contrast, in the gametophytes treated with SHAM or n-PG, A. operculata zoospores settled at higher densities (72.5 ± 6.3 and 68.6 ± 5.8 spots mm–2, respectively), and developed into invasive filaments deeply embedded in the host medullary tissue (see supplemental data).
The biological significance of oxylipin metabolism in C. crispus was further investigated by asking whether these compounds induce other defense responses in the alga. As oxylipins did not trigger an oxidative burst in C. crispus (data not shown) and since no other defense reactions have been unequivocally documented in red algae so far (Potin et al., 2002
Oxylipins Confer Induced Resistance to the Sporophytes of C. crispus
The involvement of the oxylipin pathways in the defense system of C. crispus was further investigated by incubating C. crispus sporophytes (the life-history phase susceptible to infection by the endophyte) for 24 h with those oxylipins previously shown to induce shikimate dehydrogenase and PAL activities and then inoculated with A. operculata zoospores. As shown in Figure 6, E–P and in Table I, A. operculata zoospores settled at high densities onto the control sporophytic fronds (Fig. 6E), and the pathogen filaments completely invaded the host tissue (Fig. 6M). In contrast, in the sporophytes pretreated with 12-HPETE (50 µg.mL–1), 13-HPODE (50 µg.mL–1), or MeJA (20 µg.mL–1), the infection rate was markedly reduced, with only a few infection spots (Fig. 6, F–H; Table I), and the filamentous germlings were arrested between the outer and inner cortex of the host tissue (Fig. 3, N–P). Interestingly, in the sporophytes treated with oxylipins, accumulation of blue fluorescence was visible surrounding the sites of attempted penetration by A. operculata zoospores (Fig. 6, J–L), whereas no UV-fluorescent compounds were observed in the control, susceptible sporophytes (Fig. 6I). Similar features were found associated with the innate resistance of C. crispus gametophytes to the endophyte (see supplemental data). They were not observed, however, in the gametophytes pretreated with lipoxygenase inhibitors or in the sporophytes incubated with prostaglandins (data not shown). The above findings, reminiscent of the deposition of phenolic compounds in higher plant-pathogen interactions (McLusky et al., 1999
We here show that both C20 and C18 PUFAs and hydroxylated, epoxy, and ketol derivatives were generated (Fig. 1) and that several enzyme activities of the oxidative metabolism, including LOX, were up-regulated (Figs. 2 and 4) in C. crispus gametophytes, 24 h following challenge with pathogen extracts. All of these responses were prevented by n-PG, a radical scavenger known to inhibit several enzyme activities of the fatty acid oxidation pathway (i.e. LOX, peroxidase), indicating that, as for mammalian (Parmentier et al., 2001 ) or plant (Sasaki et al., 2001) cells, this alga may be endowed by a positive feed-back loop by which oxygenated fatty acids mediate the release from membrane lipids of their own precursors by regulating the activities of lipase-like enzymes. We also show that when challenged by pathogen extracts, C. crispus gametophytes metabolize both C20 and C18 PUFAs into the corresponding hydroperoxides and derivatives (Figs. 2–4 ) and, likely, all the way down to the cyclopentenones such as prostaglandins (Fig. 3) and MeJA (see supplemental data), i.e. the ultimate products known for these oxygenation cascades in animals and higher plants, respectively. In addition, hydroperoxides derived from both C20 and C18 PUFAs induce defense enzymes in C. crispus and conferred an induced resistance to the sporophytic generation (Fig. 6; Table I), while inhibitors of fatty acid oxidation abolished the natural resistance of the gametophytic generation and the induced resistance of the sporophytic generation.
Thus, oxylipins originating from both C20 and C18 PUFAs identified in this study (Fig. 7), including 12-HPETE and 13-HPODE, respectively, appear as essential intermediates in the innate immunity of this alga. To our knowledge, this is the first demonstration that the oxylipins of marine red algae, which so far have mainly been investigated for their potential uses as pharmaceutical agents in heterologous systems, naturally act as homologous defense mediators in the phylum Rhodophyta. Further experiments are now required to identify which products of 12-HPETE and of 13-HPODE are active in C. crispus defense responses. In this respect, it is worth noting here that, even though prostaglandins B1 and B2 were produced in the elicited alga, all of the prostaglandins investigated in this study (A1, A2, B1, and B2) and which are known as major defense cyclopentenones in mammalian cells (Funk, 2001
Using cell-free homogenates of C. crispus gametophytes, we detected the presence of MeJA only after incubation with linolenic acid. Our previous attempts to identify JA in C. crispus cell homogenates using a protocol optimized for higher plants (Schittko et al., 2000 ) remained unsuccessful, and we were unable to show any up-regulation of JA synthesis after elicitation, as it is observed in elicited cells from higher plants (Howe and Schilmiller, 2002). In higher plants, it is well established that the allene oxide synthase (AOS) branch of the 13-LOX pathway gives rise to JA and MeJA, and their metabolic precursor 12-oxo-10,15-phytodienoic acid (12-OPDA; Howe and Schilmiller, 2002). AOS catalyzes the transformation of 13-hydroperoxy linolenic acid (13-HPOTE) to an allene oxide intermediate, 12,13-epoxyoctadecatrienoic acid (12,13-EOTE), which is converted to 12-OPDA by an allene oxide cyclase. Reduction of 12-OPDA by OPDA reductase and three cycles of  -oxidation then yields JA, while a carboxymethyl transferase catalyzes the formation of MeJA. During in vitro reactions carried out in the absence of allene oxide cyclase, 12,13-EOTE spontaneously hydrolyzes to - and -ketols and can also undergo nonenzymatic cyclization to produce racemic 12-OPDA (Howe and Schilmiller, 2002). Our preliminary data indicate that MeJA is produced from linolenic acid in the cell-free system from C. crispus gametophytes, implying that the pathway, which lead to the synthesis of MeJA in higher plants, may exist in marine algae. In such a crude homogenate, it is not surprising that the enzymes of -oxidation are still active. Further experiments are required to identify the different components of this pathway.
In conclusion, the red alga C. crispus is likely to use both animal-like (eicosanoid) and higher-plant-like (octadecanoid) oxylipins in the regulation of its metabolism toward protection against pathogens. This duality of the oxylipin metabolism parallels that of mammalian cells, where there is emerging evidence that, besides the C20:4 derivatives, the oxygenation products from C18:2 can act as defense compounds (Ishizaki et al., 1995a
Our findings also raise the question of which enzymes are involved with the generation of C20 and C18 cyclopentenones in red algae, either AOS as in plants and/or cyclooxygenase as in metazoans or else an enzyme machinery specific to this phylum. Presence of JA and MeJA has already been reported in several lineages of nonvascular plants (Hamberg and Gardner, 1992 ), including unicellular green algae (Ueda et al., 1991a; Fujii et al., 1997), Euglenophytes (Ueda et al., 1991b), and the Rhodophyte Gelidium latifolium (Krupina and Dathe, 1991). The entire set of enzymes necessary for the biosynthesis of JA from linolenic acid have also been identified in the marine red algae Gracilariopsis sp. (Hamberg and Gerwick, 1993) and Lithothamnion corallioides (Hamberg, 1992). In addition, JA was reported from the cyanobacterium Spirulina sp. (Ueda et al., 1991a), an AOS gene was identified in the genome of another cyanobacterium, Anabaena (www.kazusa.or.jp/cyanobase/), and the envelope membrane from higher-plant chloroplasts is known to contain the whole set of enzymes for the oxygenation of octadecanoic acid hydroperoxides (Blée and Joyard, 1996). As photosynthetic eukaryotes have arisen from a single endosymbiosis event between a heterotrophic eukaryote and a photosynthetic cyanobacterium (Baldauf et al., 2000), it is thus tempting to speculate that the ability to synthesize jasmonate was acquired from the plastid genome. That transfer of this gene to the nucleus occurred before the radiation of the green lineage (Fig. 8) would account for the occurrence of JA in both red algae and higher plants. As powerful genomic approaches are now becoming applied to gene mining in red (Nikaido et al., 2000) and other algae, sequences for enzymes involved with oxylipin biosynthesis will soon be available in these phyla, providing additional data to assess the evolution of these pathways (Brash, 1999).
Chemicals Fatty acids (C14:0, C16:0, C18:1, C18:2, C18:3, C18:4, C20:4, and C20:5) and prostaglandins A1, B1, A2, and B2 were purchased from Sigma (St. Louis); oxylipins 12-HPETE, 13-HPODE, 13-HODE, (15-, 12-, 11-, 8-) HETEs, 11,12-EET, and vernolic and coronaric acids were from Cayman Chemicals (SPI Bio, Montigny le Bretonneux, France); and MeJA from Aldrich (Milwaukee, WI). Silylating reagent N, N-bistrimethylsilyltrifluoroacetamide containing 1% of trimethylchlorosilane (BSTFA + 1% TMCS) was from Pierce Europe (Ound-Beijerland, The Netherlands). All chemicals and solvents were from Merck (Darmstadt, Germany) and Sigma.
Unialgal cultures of Acrochaete operculata (isolates P 161085-2-1 and KH 040687-1-1) were established and grown in enriched seawater medium with full concentration of nutrients (SFC) as described previously (Correa and McLachlan, 1991
Infection trials were performed as described in Bouarab et al. (1999)
Algal samples were ground in liquid nitrogen and aliquots (500 mg blotted fresh weight) were incubated at 0°C for 10 min in 2 mL of extraction buffer (50 mM Tris-HCl, pH 9.5, 500 mM KCl, and 10 mM
The metabolites from linoleic, linolenic, and arachidonic acids were resolved and characterized by RP-HPLC coupled to a Navigator LC-MS mass spectrometer (Finnigan, Manchester, UK), equipped with an atmospheric pressure ionization source (APCI) running on a negative ion mode (cone voltage 30 V and 45 V for compounds fragmentation, as detailed in Adas et al., 1998
GC-MS analyses were carried out on a HP 5890 Series II gas chromatograph equipped with a fused silica capillary column (HP-5MS 5% phenyl methyl siloxane; 30 m x 0.32 mm I.P, film thickness –0.25 µm) and combined to a quadrupole mass-selective detector (HP 5971A, Agilent Technology, Massy, France). Mass spectra (E.I. mode) were recorded at 70 eV. Analyses were performed after methylation with ethereal diazomethane and silylation with a mixture of BSTFA (N,N-bistrimethylsilyl-trifluoroacetamide)/TMCS (trimethylchlorosilane; 100:1, v/v) for 30 min at 60°C, in order to obtain trimethylsilyl derivatives for compounds containing hydroxyl group (Pinot et al., 1992
C. crispus thalli were incubated for 1 h with oxylipins at the concentration of 50 µg/mL (20 µg mL–1 for MeJA). At 24 h after treatment, proteins were extracted and the 15,000g-centrifugation supernatants were analyzed by Native-PAGE (Laemmli, 1970
We are grateful to Prof. Juan Correa for providing us with unialgal isolates of A. operculata and unialgal C. crispus strains and for his helpful advice. We are also grateful to Dr. Georg Pohnert for his attempts to assay JA in C. crispus gametophytes. We also thank Drs. John Rathjen, Des Bradley, and Peter Moffett for critical reading of the manuscript. Emmanuel Gaquerel is supported by a Ph.D. fellowship from Ministère de l'Education Nationale, de la Recherche et de la Technologie. This study has been conducted under the Programme de Recherche d'Intérêt Régional. Received December 15, 2003; returned for revision April 22, 2004; accepted April 29, 2004.
1 This work was supported by CNRS (Jeunes Equipes 2002 grant to P.P.) and by the Conseil Régional de Bretagne (grant no. PRIR–AOC429). 
2 These authors contributed equally to the paper.
3 Present address: Université de Sherbrooke, Département de Biologie, 2500 BLD de l'Université Sherbrooke, Québec J1K2R1, Canada.
[w] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.037622. * Corresponding author; e-mail potin{at}sb-roscoff.fr; fax 33–298292324.
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