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Phytohormones and Pheromones: Comparison
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Please note this is a comparison between Version 2 by Rita Xu and Version 1 by Vaibhav A. Mantri.

Plant hormones and pheromones are natural compounds involved in the growth, development, and reproductive processes. There is a plethora of studies on hormones and pheromones in terrestrial plants, but such investigations are few in the phycological literature. There are striking similarities between the chemical diversity, biosynthetic processes, roles, and actions of hormones and pheromones in both higher angiospermic plants and algae.

  • aquaculture
  • biosynthetic pathways
  • hormones
  • pheromones

1. Introduction

Algae are a diverse group of photosynthetic organisms that are unrelated ecologically as well morphologically to other groups [1]. They range from microscopic unicellular forms to large multicellular seaweeds, representing a crucial component of aquatic ecosystems, contributing significantly to oxygen production and serving as fundamental sources of nutrition [2,3][2][3]. Classified into various taxonomic groups, including green, brown, and red algae, they showcase a remarkable adaptability to diverse environments, highlighting their significance in both freshwater and marine ecosystems [4]. The forms around which considerable trade and economics are developed are marine macroalgae. They represent heterogeneous artificial groups, forms of marine polyphyletic origin, and different evolutionary lineages [5].
The perennial, multilayered seaweed stands of large ‘kelps’ represent the most productive ecosystems, which can sequester significant blue carbon and consequently increase oxygen in the oceanic environment [6]. Seaweeds have a long-standing history of exploitation by humankind for food, fodder, and agriculture, especially in Asia, Polynesia, and South America [7]. Propelled by emerging applications in day-to-day commodity products and biotechnological and medical use, seaweeds have been industrially farmed. In 2018, the commercial production of seaweeds globally reached more than 30 million tons, 97% of which was harvested through aquaculture [8]. Currently, 47 species and two varieties of 27 genera are commercially cultivated—largely in Asian countries [9]. The industry is expected to improve its performance by 12% annual growth and is anticipated to reach USD 30.2 billion by 2025 [10]. The burgeoning global population necessitated substantial improvement in food production even at the cost of limited availability of agricultural land, fast-deteriorating soil quality, shortages of water for irrigation, and protuberances by climate change. It should be noted that, considering current consumption trends, there is an urgent need to produce 50–70% additional food by 2050 [11]. The seaweeds or their extracts have been used since ancient times as soil conditioners or fertilizers in agriculture [12]. Their large-scale application has considerable potential to improve food production [13]. This is because they are needed only in small dosages—often diluted in volume by a factor of 20–500 [14]—as growth stimulants to enhance yield [15], impart disease resistance [16], elevate drought tolerance [17], reduce pest infestation [18], and improve shelf-life of produce [19]. These applications need in-depth scientific understating to unravel their mode of action, which is largely unknown. The empirical evidence showed that the growth responses elicited by seaweed extracts cannot be attributed to the presence of macro- and micro-elements alone, but plant growth regulatory compounds might also play a catalytic role [20]. The discovery of different classes of hormones in seaweeds or their extracts was evident from the work that was carried out during the late 1960s to early 1970s [21].

2. Role of Hormones in Algae

2.1. Auxin

Auxin, found in higher plants, algae, microorganisms, fungi, and animals [108[22][23],109], plays a key role in plant growth and development. Generally, the hormone concentration found in algae is much lower as compared to the higher plants [110][24]. Its function in the growth and development of algae is similar to that in higher plants [111][25]. Auxin plays a key role in cell division and elongation, suppresses branching at the apical and intercalary regions in red algae Grateloupia dichotoma [112][26], and has a significant role in the determination of zygote polarization in fucoid algae, i.e., Fucus distichus and Fucus vesiculosus [58,113][27][28]. Supplementing the axenic culture of Ulva lactuca germlings in enriched seawater with kinetin and IAA resulted in the formation of a normal flat blade, which further increased the length of the filament with the addition of gibberellin [26][29]. Similar results were also found with different algae, like Fucus spiralis, Porphyra tenera, and Enteromorpha compressa, when exogenously supplied auxins, p-hydroxy-phenylacetic acid (OH-PAA), and PAA, inducing branching and broadening of fronds [24,114,115][30][31][32]. Inhibition of apical dominance was also found in macroalgae when the apical meristem was removed or damaged, thereby inducing the growth of axillary buds and the formation of lateral branches [116][33]. IAA concentration in Caulerpa was in the same range as in angiosperms [117][34]. The activity of IAA in cultured Caulerpa triggered the initiation of leaf-like structures and slower elongation of rhizome-like structures [28][35]. The synergistic effect of IAA, kinetin, and gibberellic acid (GA) studied in Ulva lactuca induced significant growth higher than each of these hormones individually [26][29]. The role of IAA in tissue differentiation in multicellular algae has been evident in the literature, in addition to the role in cell elongation and cell division, as observed in higher plants [29][36]. IAA application also induces cell division by upregulating the genes that encode CDKs, Cycs, CDCs, and tubulins, resulting in increased branch number and promotion of rhizoid branching in Gracilariopsis lemaneiformis [118][37].

2.2. Cytokinins

Cytokinins regulate key processes like cell division and growth activation in algae just like in higher plants [82][38]. Kinetin (cytokinin) shows a positive effect on the growth of thallus when added simultaneously with GA, resulting in the formation of adventitious branches from the apical portion of Fucus vesiculosus [34][39]. Independently as well, kinetin or GA can partly replace the apical cells in Sphacelaria furcigera and increase the length of newly formed lateral branches (apical dominance) from the injured parts of the alga [31][40]. Cytokinins show less diversity in algae than higher plants but they perform a vital role in the growth and morphogenesis of algae [85][41]. Cytokinin-like activity occurred in Sargassum heterophyllum during gamete release and at the beginning of receptacle development [119][42]. Intercalary meristem of young blades of the Macrocystis pyrifera exhibit cytokinin activity in the form of free bases or ribosides and are responsible for cell division, whereas older blades contained cytokinins in the form of O-glucoside as a storage form [120][43]. Cytokinin, present in seaweed, in the form of free bases and ribosides are the physiologically active forms and can be detected in low concentrations, as they are actively utilized in several developmental processes [36][44]. Cytokinins, play an important role in the early growth of the receptacles in Sargassum muticum and are also responsible for thalli to possess mature spermatangia and carpogonia in Porphyra perforata [33][45].

2.3. Gibberellins (GAs)

The regulatory action of GA is well studied in higher plants; however, very few studies have been undertaken to understand their role in algae. In Fucus spiralis and Tetraselmis sp., just like the higher plants, the gibberellins significantly contribute to inducing tissue differentiation via cell elongation and cell division [29][36]. Such GA-like activities were also reported in Fucus vesiculosus, F. spiralis (Phaeophyceae) [121][46], and Caulerpa paspaloides (Chlorophyta) [122][47]. GA treatments of red and brown algal cultures can induce branching and control the growth of axial structures similar to the higher plants. GA3 increases the number of antheridial filaments and spermatids in Chara vulgaris, while the anti-gibberellin, in this case, AMO-1618, inhibits its effect [35][48]. Exogenous application of GA3 distinctly increases the number of adventitious branches formed on fragments from the apical parts. GA3 also shows a positive effect, in combination with kinetin, on the growth and regeneration of Fucus vesiculosus [34][39]. In contrast, GA3 inhibits the morphogenesis in the tissue culture of the red alga Grateloupia doryphora [49].

2.4. Abscisic Acid (ABA)

In higher plants, abscission of buds and leaves and dormancy in seeds is caused by ABA and can also inhibit its growth. ABA can be detected in higher concentrations during stress conditions in vascular plants [123][50]. Similarly, ABA can also be found in many algal groups during stress conditions [124][51]. However, the concentrations in algal cells are lower as compared to the higher plants [88][52]. Exogenous ABA accelerates sorus development in addition to its role as a suppressor of vegetative growth in the brown alga Laminaria [125][53]. In Laminaria, ABA regulates the transition of sporophyte from growth to the stage of propagation [78][54]. ABA levels in Dunaliella parva, Draparnaldia mutabilis, and Dunaliella acidophila increase with the increase in salinity and pH of the culture media [38,124][51][55]. Therefore, changes in endogenous ABA levels due to different environmental conditions may provide pieces of evidence for their possible roles in algae. Higher ABA in Ulva fasciata was observed when collected from a rock pool of the upper intertidal zone since it was more exposed to adverse conditions as compared to Dictyota humifusa, which was collected from a mid-intertidal zone. Therefore, ABA acts as a stress hormone in seaweeds and performs a role in growth inhibition [36][44].

2.5. Ethylene

In higher angiospermic plants, ethylene biosynthesis occurs during the ripening process, in which biosynthesis may be activated via IAA or by any other physiological stress [84][56]. Ethylene promotes cap production in Acetabularia acetabulum (as Acetabularia mediterranea) [41][57], and its precursor 1-aminocyclopropane-l-carboxylicacid (ACC) promotes cell division and cap development in Neoporphyra perforata (as Porphyra perforata) [25][58]. During sexual reproduction, ethylene regulates gamete formation and protects against stress-induced damage in Neopyropia yezoensis, whereas its precursor, 1-aminocylopropane-1-carboxylic acid, regulates sexual reproduction by inducing the gametophytes to form spermatangia in Neopyropia yezoensis [126,127][59][60]. Ethylene also plays a key role in cell wall metabolism, photosynthesis, and abiotic stress responses in Spirogyra pratensis [128][61].

2.6. Brassinosteroids (BRs)

Brassinosteroids are polyhydroxylated steroid hormones with ubiquitous distribution that regulate the growth and development of higher angiospermic plants. The first report of Brassinosteroids viz, brassinolide (BR), and castasterone (CS) from algae was from the extract of Ecklonia maxima [42][62]. BRs stimulate the cell division and growth in Chlorella vulgaris, mostly influencing the number of algal cells, phosphorus, chlorophyll, and monosaccharide content in this alga [129][63]. In Chlorella vulgaris, BRs can regulate protein and lipid content, thereby enhancing the energy storage capacity of the alga during stress conditions like high temperatures [130,131][64][65]. It can also boost the stress-responsive ABA content with temperature rise [132][66]. BRs also play an important role during stress and defense, either individually or along with the primary defense hormones [133][67].

2.7. Jasmonic Acid (JA)

Jasmonic acid is one of the primary plant defense hormones in addition to SA and ethylene [134][68]. JA and its derivatives play a vital role as hormones and can induce defense responses by producing oxylipins (defense mediators) and prostaglandins (defense chemicals against grazers) in the red macroalga Chondrus crispus [44][69]. However, contradictory observations have been made, which suggested that JA- and methyl jasmonate (MeJA)-like compounds may be active just in higher plants and do not play any role in the algal defense system. JA and MeJA may not be ubiquitous in all red algae, as none were detected in the Gracilaria chilensis even after exposure to pathogen attack [135][70]. Therefore, the role of JA in algae needs to be re-evaluated extensively using the latest analytical techniques on various algal taxa.

2.8. Polyamines (PAs)

The polyamine biosynthetic pathway is conserved in bacteria, animals, and higher angiospermic plants [136][71]. Polyamines play an important role in physiological metabolism, which eliminates the active oxygen-free radicals, giving the plant tolerance to oxidative stresses [137][72]. Consequently, polyamines like putrescine and spermidine can help in the acclimation due to the oxidative stress caused by hyposaline conditions in green macroalga Ulva fasciata [47][73]. Similarly, in the red alga Grateloupia doryphora, during hyposaline shock, the level of putrescine, spermidine, and spermine rises, which has been attributed mainly to the decrease in transglutaminase activity [48][74]. Exogenous application of PAs can lead to effects similar to 2,4-D in Grateloupia and plays an important role in the development of cystocarp and in the release and development of spores in cultivated species of red macroalga Grateloupia sp. [49,51][49][75]. Putrescine and spermidine also play important roles in the transformation of the carposporelings into cell masses that produce shoots. Furthermore, the combination of putrescine, spermidine, and spermine leads to the formation of bigger sizes of cell masses and ultimately to a higher amount of shoot per cell mass [49]. These three are ubiquitous aliphatic amines that are also involved in reproduction in higher angiospermic plants and algae. A higher level of PA (putrescine) in immature cystocarps as compared to mature cystocarps of Crassiphycus corneus (as Gracilaria cornea) was observed, which declined in the transition event of reproduction from the infertile to the fertile state [52,53][76][77]. These reports suggest the involvement of polyamines in the reproductive events and other cellular processes in the algae as well.

2.9. Salicylic Acid (SA)

Salicylic acid (SA) is best known for mediating host responses against pathogen infection as it plays an important role in eliciting the defense responses [138][78]. Some evidence shows that SA plays an important role in the oxidative defense for protection against environmental stresses in seaweeds in a similar way as found in higher plants. SA treated Saccharina japonica (as Laminaria japonica) sporophytes before heat stress improved their thermotolerance by altering antioxidant enzymatic activity with increased superoxidase dismutase (SOD), peroxidase (POD), and catalase (CAT) activity [79].

2.10. Strigolactone (SL)

Strigolactones (SLs) are the newly categorized phytohormones that regulate plant growth, development, and metabolism. Strigolactones have been linked to a variety of physiological processes such as seed germination, nodulation, inhibition of bud outgrowth and shoot branching, photomorphogenesis, and physiological responses to abiotic stimuli [139][80]. SLs are present in basal Embryophytes, where they are involved in signaling role promoting the arbuscular mycorrhizal (AM) symbiosis [140][81]. This hypothesis, however, can be challenged by the fact that Charales, which do not participate in AM symbiosis, also synthesize and exude SLs into the medium. Such evidence, supported by sequence and metabolite profile, concluded that the widespread existence of SLs in the green lineage was probably more hormonal than symbiotic [23][82]. The closest freshwater green algal relatives of land plants, Charales, produce and exude strigolactones, which help them to survive fungal colonization. It was also proven experimentally that the exogenous SLs stimulate rhizoid elongation in Chara coralina [23][82]. Based on the literature survey, it has been suggested that strigolactones are not found in marine macroalgae. But, the lack of complete genome sequences for lower-order plants, including marine macroalgae, may make such assumptions difficult [141][83]. However, the strigolactones have been found in the liquid seaweed extract (Seasol™, Seasol International Pty Ltd, Bayswater, Australia), which is made from the biomass of Durvillaea potatorum and Ascophyllum nodosum, which have extensive applications in agriculture [142][84].

2.11. Rhodomorphin

Rhodomorphin is produced by rhizoidal cells in Griffithsia pacifica, a red alga [139][80], and is a species-specific growth regulator [21]. A study on Griffithsia sp. revealed its role in the repair of rhizoids, decapitated filament, and its elongation, but no such role has been observed in shoot cell repair [39,143][85][86].

3. Role of Pheromones in Algae

3.1. Sporulation Inhibitors

Axenic culture of Ulva mutabilis produces two such inhibitors. Sporulation inhibitor-1a (SI-1a), which is a glycoprotein, is produced by their cell wall, and Sporulation inhibitor (SI-2), which is a non-protein, is produced in the space between the two blade cell layers. Both SI-1 and SI-2 play important roles in keeping the thalli in a vegetative state by suppressing gametogenesis. The absence or removal of these sporulation inhibitors causes induction in gametogenesis from the mature blades in Ulva mutabilis [60][87].

3.2. Swarming Inhibitors

Swarming inhibitors act as regulatory factors during gametogenesis and are excreted during the determination phase of the gametes and can inhibit the gamete formation event in Ulva compressa (as Ulva mutabilis) [60,144][87][88].

3.3. Ectocarpene

Ectocarpene is a chemoattractant hydrocarbon released by female gametes to attract its male counterparts [61][89]. In most of the brown algae, the fertilization is boosted by such chemical messengers. Ectocarpene is also released by female gametes of Chorda tomentosa to attract male gametes [69][90]. Ectocarpene is the first reported pheromone in brown algae Ectocarpus siliculosus and is known to induce chemokinesis. It has also been reported in Sphacelaria rigidula, Adenocystis utricularis [63][91], and in Ectocarpus fasciculatus [62][92].

3.4. Dictyotene and C11 Sulfur Compounds

Dictyotene and other C11 compounds generally found in brown algae can perform functions like saving the spores, zygotes, and germlings against mesograzers like amphipods [68][93]. These compounds and their free products also play an essential role in the chemoattraction of gametes in addition to keeping the mesograzers away from the developing zygotes. These are the volatile compounds, reported mainly in Dictyota diemensis, Dictyota dichotoma, Dictyopteris membranacea, D. delicatula, and Sargassum filipendula [64,65,66,67][94][95][96][97]. Volvox is reported to produce protein erogens; similarly, Allomyces and brown algae have been reported to secrete terpenoids and hydrophobic hydrocarbons, respectively. In Dictyota diemensis, dictyotene has also been reported to act as erotactins, the compounds attracting sperms [74][98].

3.5. Ochtodene

It is a monoterpene pheromone reported from the Ochtodes secundiramea, which protects this alga against predation by many rapacious herbivores. It also has antibacterial activity against Staphylococcus aureus. Therefore, its antimicrobial role is also important [76][99].

4. Mode of Action of Hormones in Algae

Certain plant/algal hormones, unlike animal hormones, have multiple physiological functions [145][100]. They are produced in cells and then bind to specific receptor proteins to carry out downstream signaling. Their liaison results in a change in cell function and the activation of a signal transduction pathway. The concentration of individual hormones is not important, but the response of hormones is usually governed by the sum effect of other hormones either in tandem or vice versa [146][101]. In higher angiospermic plants, auxin signal may be perceived at the extracellular matrix, at ER, or inside the nucleus with the help of a receptor ABP1 (Auxin-Binding Protein1) [147,148][102][103]. ABP1 homologs have also been found in genomes of Chlorella variabilis NC64A, Chlorella pyrenoidosa, and Chlamydomonas reinhardtii. These proteins form the auxin-binding pocket, which in the presence of auxin, induces transcription of auxin responsive genes [149][104]. These findings suggest the early emergence of a primitive form of auxin receptors in microalgae [150][105]. Additionally, more genome sequences of a variety of algae are required to elucidate the origin of auxin signaling in them. Cytokinin signaling involves the phosphorylation of cytokinin, which binds to the extracellular portion of cytokinin response1 (CRE1), known as the CHASE domain, localized at the plasma membrane [84][56]. The cytokinin signaling components have evolved in microalgae, and further analogous evolution occurred among different algal lineages [150][105]. In Arabidopsis, cytokinin is perceived by AHK receptors located in the endoplasmic reticulum, triggering their histidine kinase activity [151][106]. These receptors are also common in the algal genome [152][107]. This histidine kinase activity leads to a cascade of phosphorylation from the cytoplasm to the nucleus, ultimately activating the transcription of type-A Arabidopsis Response Regulators (ARRs) and CRFs. Homologous components of these proteins (type-B Arabidopsis Response Regulators and Histidine-Containing Phosphotransmitter 1) have also been found in green microalgae (Nannochloropsis oceanica), suggesting the similarities in their mode of action in microalgae (Nannochloropsis) and plant (Arabidopsis) [152][107]. The phosphorylated type-A ARRs then interact with various effectors to bring about cytokinin responses [84,151][56][106]. Gibberellic acid (GA) molecules bind to the GID1 (GIBBERELLIN INSENSITIVE DWARF1) receptor in higher angiospermic plants, which then interacts with DELLA proteins [153][108]. DELLA proteins interact with DNA-binding proteins, which are regulated by PIFs (Phytochrome-Interacting Factors) [154][109]. GID1 receptor orthologs have been identified in microalgae via the functional motif analysis and revealed that the GID homologs have the catalytic triad (S, D, and H) of the hormone-sensitive lipase (HSL) family in microalgae [150][105]. Therefore, this supports the inheritance of GA signaling from microalgae, which might be the crucial source for the foundations of the higher plant hormone systems. However, some proteins (DELLA and the F-box protein SLEEPY1) involved in mediating GA signaling have been found only in land plants and not in microalgae [155][110]. This warrants a thorough exploration of downstream signaling molecules involved in GA [150][105]. Three abscisic acid (ABA) receptors have been identified in higher angiospermic plants, i.e., chloroplast envelope-localized ABA receptor (ChlH/ABAR), plasma membrane-localized GTG1/GTG2 (GPCR-type G protein 1 and 2), and nucleo-cytoplasmic PYR/PYL/RCARs (pyrabactin resistance/pyrabactin resistance-like/regulatory component of ABA receptors) [156,157][111][112]. Among these, the nucleo-cytoplasmic PYR/PYL/RCAR receptors are considered the most established ABA perception receptors. These receptors have not been identified in microalgae to date, even though the downstream phosphatases (SNF1-Related Protein Kinase 2) of the ABA signaling pathway are conserved from microalgae to higher plants [158][113]. Nevertheless, ABA-related genes in algae have not been explored, and it is necessary to compare them to gain more definite proof of the evolutionary origin of ABA-related genes [159][114]. Ethylene perception in higher angiospermic plants occurs through membrane-bound receptors embedded in the endoplasmic reticulum (ER). Arabidopsis has five known ethylene receptors, which are ETR1 (Ethylene Response1), ETR2, ERS1 (Ethylene Response Sensor1), ERS2, and EIN4 (Ethylene Insensitive 4) [160][115]. Ethylene receptor complexes, comprising ETR1, ERS, and EIN4, have been widely reported in microalgae (Micromonas sp.) [150][105]. In addition to that, ethylene binding sites have also been confirmed in a cyanobacterial protein [161][116]. In silico genome-wide homology search analysis revealed the biosynthetic pathways of iP and ABA in red seaweeds similar to those in terrestrial plants. However, the mode of action in these seaweeds (Neopyropia yezoensis and Bangia fuscopurpurea) are dissimilar to those in terrestrial plants for IAA, iP, and ABA [162][117] and are yet to be investigated. Hormones like brassinosteroids (BRs), jasmonic acid, salicylic acid, and rhodomorphin have been reported from algae, but their possible signaling mechanism is yet to be investigated [54,141,163][83][118][119].

5. Mode of Action of Pheromones in Algae

Green algae undergo sexual reproduction during their life cycle to survive unfavorable environmental conditions. Induction of gametogenesis in Chlamydomonas reinhardtii is activated via a reduced nitrogen supply in the environment [164][120]. After gametogenesis, the agglutinins, sex-specific glycoproteins located on the flagella, are synthesized, which promotes the interactions between different mating types and may lead to their fusion [165][121]. The gamete fusion takes place only when two compatible gametes come in contact with each other [164][120]. This contact induces the production of certain enzymes, which facilitate their fusion and form a cell having four flagella, ultimately giving rise to a non-motile zygote [96][122]. The attraction between the gametes and the level of compatibility between cells in C. reinhardtii decides the mating success. Similarly, in other species of Chlamydomonas, chemotactic behavior of gametes can be observed [74][98]. At low concentrations of pheromone lurlene, motile MT− gametes of Chlamydomonas allensworthii attract the motile MT+ gametes [166][123]. In Volvox carteri f. nagariensis, the male clones produce inducer molecules, extracellular matrix (ECM) glycoproteins called pherophorins, which can control sexualization. This protein is originally of somatic origin but can induce the production of respective gametes in both male and female algae [167,168][124][125]. After the gamete production, the sperm cells attain the ability to produce this inducer, which is now called pheromone [169][126]. The release of this pheromone can also lead to the production of hydroxyproline. Remarkably, the wounding of Volvox also produces a similar protein. Such expression of the same genes, which are activated by the wounding as well as pheromone induction, hints toward an existing relationship between environmental stress, sexual reproduction, and wound healing at the molecular level [170][127]. The blade cells of green macroalga Ulva mutabilis secrete some regulatory factors, which control the gametogenesis and are important to keep its thallus in a vegetative state. One of these factors, a sporulation inhibitor, prevents the differentiation of blade cells into gametangia [60][87]. During the maturation of the thallus, the production of this factor gradually decreases and stops until the concentration drops to the inhibitory concentration of 10−14 M. At this point, another sporulation inhibitor is released into the environment, which can supposedly control the distribution of gametangia spatially while they are developing. After induction, a swarming inhibitor is produced, which inhibits the release of gametes from U. mutabilis and U. lactuca [96][122]. Ectocarpene was identified as the first male-attracting chemical released by female plants. It was the first identified from Ectocarpus siliculosus. The compound is apolar and derived from a fatty acid, 9-hydroperoxyicosa (5Z,7E,11Z,14Z,17Z)-pentaenoic acid [61][89]. This compound is formed after the precursor is subjected to thermal rearrangement [104][128]. The inactivation process is wholly controlled by temperature and does not require any enzymatic activity [96][122]. Ectocarpene functions as a chemoattractant not only in many Ectocarpus species [62][92] but also in other brown algal genera like Adenocystis and Sphacelaria [63][91]. However, it has not yet been determined if the ectocarpene is as native in these species as in E. siliculosus. The gamete recognition and union in this alga is mediated by the lectin–glycoprotein complexes present in the membranes [171][129]. In another example, a structurally related epoxidized hydrocarbon from Laminaria digitata synchronizes the release of male gametes [172][130]. In marine brown algae Hormosira banksiii, Durvillea sp., Xiphophora sp., Scytosiphon lomentaria, and Colpomenia perergrina, chemical signal hormosirene was found to be released by female gametes (1–1000 pmol) to attract their conspecific male gametes [104][128]. Various life cycle stages of Giffordia mitchellae produce odoriferous compounds comprising mainly of giffordene and its stereoisomers because its male gametes are strongly attracted to settled female gametes [98][131]. In the orders Laminariales, Sporochnales, and Desmarestiales, sexual pheromones induce spermatozoid release from antheridia. In Laminaria, Maier et al. summarized the regulation of sexual reproduction by pheromones and other environmental factors [173][132]. The chemotactic movement of spermatozoids of Hormosira banksii and Laminaria digitata has also been reported in the literature [174,175][133][134]. Wirth and Boland recognized spermatozoid-attracting and spermatozoid-releasing factors in Perithalia caudata [176][135]. The interactions between various receptor–pheromone complexes have been studied in many species utilizing a number of pheromone analogs synthesized chemically [173][132]. But still, there seems to be no clarity on the molecular nature and cellular localization of various pheromone receptors. The first stage in the binding of brown algal pheromones is probably the partitioning into the cellular membrane due to the hydrophobic nature of this compound. Binding to the receptor protein strongly depends on the steric characteristics of the pheromone molecules and is intermediated by non-covalent dispersion forces, like how the double bonds are arranged in the molecule [74][98]. In chemotaxis assays, the binding process involves a strict enantiomer differentiation, which occurs as per the enantiomer specificity; the higher the specificity, the better the binding. Boland et al. hypothesized computer scheming for the identification of minimum energy conformations and a receptor-bound metal cation acting as the coordination center in pheromone binding [177][136].

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