REVIEW   Open Access    

Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products

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  • Fish and fish products offer a wide variety of nutritional and health benefits, thanks to the desirable protein and quality. Nevertheless, their quality is prone to degradation due to microbial contamination, oxidation and enzymatic reactions during the storage period. This results in the development of unsuitable flavor and rancid odor hence affecting the freshness, texture and sensory acceptability. Various processing methods such as drying, chilling, freezing etc. are employed, but they seemed to be insufficient to prevent such deterioration. Therefore, additives are added to maintain and/or improve the quality and extend the shelf-life of muscle foods, including fish products. In recent years, natural food additives are well perceived by consumers over synthetic ones. Perceived naturalness is mainly related to healthiness. Natural products, such as plant-derived phytochemicals (phenolics, essential oils, carotenoids, lignins and other molecules), having antioxidant and antimicrobial properties offer plenty of opportunities to overcome protein degradation, lipid peroxidation and also to inhibit microbial growth, thereby improving the quality and shelf-life of food products. This review intends to critically address the potential of phytochemicals as natural food additives to prevent the deterioration of the quality and safety of fish products, and thus providing healthy and safe final products to the consumers.
  • As a major staple crop, today maize accounts for approximately 40% of total worldwide cereal production (http://faostat.fao.org/). Since its domestication ~9,000 years ago from a subgroup of teosinte (Zea mays ssp. parviglumis) in the tropical lowlands of southwest Mexico[1], its cultivating area has greatly expanded, covering most of the world[2]. Human's breeding and utilization of maize have gone through several stages, from landraces, open-pollinated varieties (OPVs), double-cross hybrids (1930s-1950s) and since the middle 1950s, single-cross hybrids. Nowadays, global maize production is mostly provided by single-cross hybrids, which exhibit higher-yielding and better stress tolerance than OPVs and double-cross hybrids[3].

    Besides its agronomic importance, maize has also been used as a model plant species for genetic studies due to its out-crossing habit, large quantities of seeds produced and the availability of diverse germplasm. The abundant mutants of maize facilitated the development of the first genetic and cytogenetic maps of plants, and made it an ideal plant species to identify regulators of developmental processes[46]. Although initially lagging behind other model plant species (such as Arabidopsis and rice) in multi-omics research, the recent rapid development in sequencing and transformation technologies, and various new tools (such as CRISPR technologies, double haploids etc.) are repositioning maize research at the frontiers of plant research, and surely, it will continue to reveal fundamental insights into plant biology, as well as to accelerate molecular breeding for this vitally important crop[7, 8].

    During domestication from teosinte to maize, a number of distinguishing morphological and physiological changes occurred, including increased apical dominance, reduced glumes, suppression of ear prolificacy, increase in kernel row number, loss of seed shattering, nutritional changes etc.[9] (Fig. 1). At the genomic level, genome-wide genetic diversity was reduced due to a population bottleneck effect, accompanied by directional selection at specific genomic regions underlying agronomically important traits. Over a century ago, Beadle initially proposed that four or five genes or blocks of genes might be responsible for much of the phenotypic changes between maize and teosinte[10,11]. Later studies by Doebley et al. used teosinte–maize F2 populations to dissect several quantitative trait loci (QTL) to the responsible genes (such as tb1 and tga1)[12,13]. On the other hand, based on analysis of single-nucleotide polymorphisms (SNPs) in 774 genes, Wright et al.[14] estimated that 2%−4% of maize genes (~800−1,700 genes genome-wide) were selected during maize domestication and subsequent improvement. Taking advantage of the next-generation sequencing (NGS) technologies, Hufford et al.[15] conducted resequencing analysis of a set of wild relatives, landraces and improved maize varieties, and identified ~500 selective genomic regions during maize domestication. In a recent study, Xu et al.[16] conducted a genome-wide survey of 982 maize inbred lines and 190 teosinte accession. They identified 394 domestication sweeps and 360 adaptation sweeps. Collectively, these studies suggest that maize domestication likely involved hundreds of genomic regions. Nevertheless, much fewer domestication genes have been functionally studied so far.

    Figure 1.  Main traits of maize involved in domestication and improvement.

    During maize domestication, a most profound morphological change is an increase in apical dominance, transforming a multi-branched plant architecture in teosinte to a single stalked plant (terminated by a tassel) in maize. The tillers and long branches of teosinte are terminated by tassels and bear many small ears. Similarly, the single maize stalk bears few ears and is terminated by a tassel[9,12,17]. A series of landmark studies by Doebley et al. elegantly demonstrated that tb1, which encodes a TCP transcription factor, is responsible for this transformation[18, 19]. Later studies showed that insertion of a Hopscotch transposon located ~60 kb upstream of tb1 enhances the expression of tb1 in maize, thereby repressing branch outgrowth[20, 21]. Through ChIP-seq and RNA-seq analyses, Dong et al.[22] demonstrated that tb1 acts to regulate multiple phytohormone signaling pathways (gibberellins, abscisic acid and jasmonic acid) and sugar sensing. Moreover, several other domestication loci, including teosinte glume architecture1 (tga1), prol1.1/grassy tillers1, were identified as its putative targets. Elucidating the precise regulatory mechanisms of these loci and signaling pathways will be an interesting and rewarding area of future research. Also worth noting, studies showed that tb1 and its homologous genes in Arabidopsis (Branched1 or BRC1) and rice (FINE CULM1 or FC1) play a conserved role in repressing the outgrowth of axillary branches in both dicotyledon and monocotyledon plants[23, 24].

    Teosinte ears possess two ranks of fruitcase-enclosed kernels, while maize produces hundreds of naked kernels on the ear[13]. tga1, which encodes a squamosa-promoter binding protein (SBP) transcription factor, underlies this transformation[25]. It has been shown that a de novo mutation occurred during maize domestication, causing a single amino acid substitution (Lys to Asn) in the TGA1 protein, altering its binding activity to its target genes, including a group of MADS-box genes that regulate glume identity[26].

    Prolificacy, the number of ears per plants, is also a domestication trait. It has been shown that grassy tillers 1 (gt1), which encodes an HD-ZIP I transcription factor, suppresses prolificacy by promoting lateral bud dormancy and suppressing elongation of the later ear branches[27]. The expression of gt1 is induced by shading and requires the activity of tb1, suggesting that gt1 acts downstream of tb1 to mediate the suppressed branching activity in response to shade. Later studies mapped a large effect QTL for prolificacy (prol1.1) to a 2.7 kb 'causative region' upstream of the gt1gene[28]. In addition, a recent study identified a new QTL, qEN7 (for ear number on chromosome 7). Zm00001d020683, which encodes a putative INDETERMINATE DOMAIN (IDD) transcription factor, was identified as the likely candidate gene based on its expression pattern and signature of selection during maize improvement[29]. However, its functionality and regulatory relationship with tb1 and gt1 remain to be elucidated.

    Smaller leaf angle and thus more compact plant architecture is a desired trait for modern maize varieties. Tian et al.[30] used a maize-teosinte BC2S3 population and cloned two QTLs (Upright Plant Architecture1 and 2 [UPA1 and UPA2]) that regulate leaf angle. Interestingly, the authors showed that the functional variant of UPA2 is a 2-bp InDel located 9.5 kb upstream of ZmRAVL1, which encodes a B3 domain transcription factor. The 2-bp Indel flanks the binding site of the transcription factor Drooping Leaf1 (DRL1)[31], which represses ZmRAVL1 expression through interacting with Liguleless1 (LG1), a SBP-box transcription factor essential for leaf ligule and auricle development[32]. UPA1 encodes brassinosteroid C-6 oxidase1 (brd1), a key enzyme for biosynthesis of active brassinolide (BR). The teosinte-derived allele of UPA2 binds DRL1 more strongly, leading to lower expression of ZmRAVL1 and thus, lower expression of brd1 and BR levels, and ultimately smaller leaf angle. Notably, the authors demonstrated that the teosinte-derived allele of UPA2 confers enhanced yields under high planting densities when introgressed into modern maize varieties[30, 33].

    Maize plants exhibit salient vegetative phase change, which marks the vegetative transition from the juvenile stage to the adult stage, characterized by several changes in maize leaves produced before and after the transition, such as production of leaf epicuticular wax and epidermal hairs. Previous studies reported that Glossy15 (Gl15), which encodes an AP2-like transcription factor, promotes juvenile leaf identity and suppressing adult leaf identity. Ectopic overexpression of Gl15 causes delayed vegetative phase change and flowering, while loss-of-function gl15 mutant displayed earlier vegetative phase change[34]. In another study, Gl15 was identified as a major QTL (qVT9-1) controlling the difference in the vegetative transition between maize and teosinte. Further, it was shown that a pre-existing low-frequency standing variation, SNP2154-G, was selected during domestication and likely represents the causal variation underlying differential expression of Gl15, and thus the difference in the vegetative transition between maize and teosinte[35].

    A number of studies documented evidence that tassels replace upper ears1 (tru1) is a key regulator of the conversion of the male terminal lateral inflorescence (tassel) in teosinte to a female terminal inflorescence (ear) in maize. tru1 encodes a BTB/POZ ankyrin repeat domain protein, and it is directly targeted by tb1, suggesting their close regulatory relationship[36]. In addition, a number of regulators of maize inflorescence morphology, were also shown as selective targets during maize domestication, including ramosa1 (ra1)[37, 38], which encodes a putative transcription factor repressing inflorescence (the ear and tassel) branching, Zea Agamous-like1 (zagl1)[39], which encodes a MADS-box transcription factor regulating flowering time and ear size, Zea floricaula leafy2 (zfl2, homologue of Arabidopsis Leafy)[40, 41], which likely regulates ear rank number, and barren inflorescence2 (bif2, ortholog of the Arabidopsis serine/threonine kinase PINOID)[42, 43], which regulates the formation of spikelet pair meristems and branch meristems on the tassel. The detailed regulatory networks of these key regulators of maize inflorescence still remain to be further elucidated.

    Kernel row number (KRN) and kernel weight are two important determinants of maize yield. A number of domestication genes modulating KRN and kernel weight have been identified and cloned, including KRN1, KRN2, KRN4 and qHKW1. KRN4 was mapped to a 3-kb regulatory region located ~60 kb downstream of Unbranched3 (UB3), which encodes a SBP transcription factor and negatively regulates KRN through imparting on multiple hormone signaling pathways (cytokinin, auxin and CLV-WUS)[44, 45]. Studies have also shown that a harbinger TE in the intergenic region and a SNP (S35) in the third exon of UB3 act in an additive fashion to regulate the expression level of UB3 and thus KRN[46].

    KRN1 encodes an AP2 transcription factor that pleiotropically affects plant height, spike density and grain size of maize[47], and is allelic to ids1/Ts6 (indeterminate spikelet 1/Tassel seed 6)[48]. Noteworthy, KRN1 is homologous to the wheat domestication gene Q, a major regulator of spike/spikelet morphology and grain threshability in wheat[49].

    KRN2 encodes a WD40 domain protein and it negatively regulates kernel row number[50]. Selection in a ~700-bp upstream region (containing the 5’UTR) of KRN2 during domestication resulted in reduced expression and thus increased kernel row number. Interestingly, its orthologous gene in rice, OsKRN2, was shown also a selected gene during rice domestication to negatively regulate secondary panicle branches and thus grain number. These observations suggest convergent selection of yield-related genes occurred during parallel domestication of cereal crops.

    qHKW1 is a major QTL for hundred-kernel weight (HKW)[51]. It encodes a CLAVATA1 (CLV1)/BARELY ANY MERISTEM (BAM)-related receptor kinase-like protein positively regulating HKW. A 8.9 Kb insertion in its promoter region was find to enhance its expression, leading to enhanced HKW[52]. In addition, Chen et al.[53] reported cloning of a major QTL for kernel morphology, qKM4.08, which encodes ZmVPS29, a retromer complex component. Sequencing and association analysis revealed that ZmVPS29 was a selective target during maize domestication. They authors also identified two significant polymorphic sites in its promoter region significantly associated with the kernel morphology. Moreover, a strong selective signature was detected in ZmSWEET4c during maize domestication. ZmSWEET4c encodes a hexose transporter protein functioning in sugar transport across the basal endosperm transfer cell layer (BETL) during seed filling[54]. The favorable alleles of these genes could serve as valuable targets for genetic improvement of maize yield.

    In a recent effort to more systematically analyze teosinte alleles that could contribute to yield potential of maize, Wang et al.[55] constructed four backcrossed maize-teosinte recombinant inbred line (RIL) populations and conducted detailed phenotyping of 26 agronomic traits under five environmental conditions. They identified 71 QTL associated with 24 plant architecture and yield related traits through inclusive composite interval mapping. Interestingly, they identified Zm00001eb352570 and Zm00001eb352580, both encode ethylene-responsive transcription factors, as two key candidate genes regulating ear height and the ratio of ear to plant height. Chen et al.[56] constructed a teosinte nested association mapping (TeoNAM) population, and performed joint-linkage mapping and GWAS analyses of 22 domestication and agronomic traits. They identified the maize homologue of PROSTRATE GROWTH1, a rice domestication gene controlling the switch from prostrate to erect growth, is also a QTL associated with tillering in teosinte and maize. Additionally, they also detected multiple QTL for days-to-anthesis (such as ZCN8 and ZmMADS69) and other traits (such as tassel branch number and tillering) that could be exploited for maize improvement. These lines of work highlight again the value of mining the vast amounts of superior alleles hidden in teosinte for future maize genetic improvement.

    Loss of seed shattering was also a key trait of maize domestication, like in other cereals. shattering1 (sh1), which encodes a zinc finger and YABBY domain protein regulating seed shattering. Interesting, sh1 was demonstrated to undergo parallel domestication in several cereals, including rice, maize, sorghum, and foxtail millet[57]. Later studies showed that the foxtail millet sh1 gene represses lignin biosynthesis in the abscission layer, and that an 855-bp Harbinger transposable element insertion in sh1 causes loss of seed shattering in foxtail millet[58].

    In addition to morphological traits, a number of physiological and nutritional related traits have also been selected during maize domestication. Based on survey of the nucleotide diversity, Whitt et al.[59] reported that six genes involved in starch metabolism (ae1, bt2, sh1, sh2, su1 and wx1) are selective targets during maize domestication. Palaisa et al.[60] reported selection of the Y1 gene (encoding a phytoene synthase) for increased nutritional value. Karn et al.[61] identified two, three, and six QTLs for starch, protein and oil respectively and showed that teosinte alleles can be exploited for the improvement of kernel composition traits in modern maize germplasm. Fan et at.[62] reported a strong selection imposed on waxy (wx) in the Chinese waxy maize population. Moreover, a recent exciting study reported the identification of a teosinte-derived allele of teosinte high protein 9 (Thp9) conferring increased protein level and nitrogen utilization efficiency (NUE). It was further shown that Thp9 encodes an asparagine synthetase 4 and that incorrect splicing of Thp9-B73 transcripts in temperate maize varieties is responsible for its diminished expression, and thus reduced NUE and protein content[63].

    Teosintes is known to confer superior disease resistance and adaptation to extreme environments (such as low phosphorus and high salinity). de Lange et al. and Lennon et al.[6466] reported the identification of teosinte-derived QTLs for resistance to gray leaf spot and southern leaf blight in maize. Mano & Omori reported that teosinte-derived QTLs could confer flooding tolerance[67]. Feng et al.[68] identified four teosinte-derived QTL that could improve resistance to Fusarium ear rot (FER) caused by Fusarium verticillioides. Recently, Wang et al.[69] reported a MYB transcription repressor of teosinte origin (ZmMM1) that confers resistance to northern leaf blight (NLB), southern corn rust (SCR) and gray leaf spot (GLS) in maize, while Zhang et al.[70] reported the identification of an elite allele of SNP947-G ZmHKT1 (encoding a sodium transporter) derived from teosinte can effectively improve salt tolerance via exporting Na+ from the above-ground plant parts. Gao et al.[71] reported that ZmSRO1d-R can regulate the balance between crop yield and drought resistance by increasing the guard cells' ROS level, and it underwent selection during maize domestication and breeding. These studies argue for the need of putting more efforts to tapping into the genetic resources hidden in the maize’s wild relatives. The so far cloned genes involved in maize domestication are summarized in Table 1. Notably, the enrichment of transcription factors in the cloned domestication genes highlights a crucial role of transcriptional re-wiring in maize domestication.

    Table 1.  Key domestication genes cloned in maize.
    GenePhenotypeFunctional annotationSelection typeCausative changeReferences
    tb1Plant architectureTCP transcription factorIncreased expression~60 kb upstream of tb1 enhancing expression[1822]
    tga1Hardened fruitcaseSBP-domain transcription factorProtein functionA SNP in exon (K-N)[25, 26]
    gt1Plant architectureHomeodomain leucine zipperIncreased expressionprol1.1 in 2.7 kb upstream of the promoter region increasing expression[27, 28]
    Zm00001d020683Plant architectureINDETERMINATE DOMAIN transcription factorProtein functionUnknown[29]
    UPA1Leaf angleBrassinosteroid C-6 oxidase1Protein functionUnknown[30]
    UPA2Leaf angleB3 domain transcription factorIncreased expressionA 2 bp indel in 9.5 kb upstream of ZmRALV1[30]
    Gl15Vegetative phase changeAP2-like transcription factorAltered expressionSNP2154: a stop codon (G-A)[34, 35]
    tru1Plant architectureBTB/POZ ankyrin repeat proteinIncreased expressionUnknown[36]
    ra1Inflorescence architectureTranscription factorAltered expressionUnknown[37, 38]
    zflPlant architectureTranscription factorAltered expressionUnknown[40, 41]
    UB3Kernel row numberSBP-box transcription factorAltered expressionA TE in the intergenic region;[4446]
    SNP (S35): third exon of UB3
    (A-G) increasing expression of UB3 and KRN
    KRN1/ids1/Ts6Kernel row numberAP2 Transcription factorIncreased expressionUnknown[47, 48]
    KRN2Kernel row numberWD40 domainDecreased expressionUnknown[50]
    qHKW1Kernel row weightCLV1/BAM-related receptor kinase-like proteinIncreased expression8.9 kb insertion upstream of HKW[51, 52]
    ZmVPS29Kernel morphologyA retromer complex componentProtein functionTwo SNPs (S-1830 and S-1558) in the promoter of ZmVPS29[53]
    ZmSWEET4cSeed fillingHexose transporterProtein functionUnknown[54]
    ZmSh1ShatteringA zinc finger and YABBY transcription factorProtein functionUnknown[57, 58]
    Thp9Nutrition qualityAsparagine synthetase 4 enzymeProtein functionA deletion in 10th intron of Thp9 reducing NUE and protein content[63]
    ZmMM1Biotic stressMYB Transcription repressorProtein functionUnknown[69]
    ZmHKT1Abiotic stressA sodium transporterProtein functionSNP947-G: a nonsynonymous variation increasing salt tolerance[70]
    ZmSRO1d-RDrought resistance and productionPolyADP-ribose polymerase and C-terminal RST domainProtein functionThree non-synonymous variants: SNP131 (A44G), SNP134 (V45A) and InDel433[71]
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    After its domestication from its wild progenitor teosinte in southwestern Mexico in the tropics, maize has now become the mostly cultivated crop worldwide owing to its extensive range expansion and adaptation to diverse environmental conditions (such as temperature and day length). A key prerequisite for the spread of maize from tropical to temperate regions is reduced photoperiod sensitivity[72]. It was recently shown that CENTRORADIALIS 8 (ZCN8), an Flowering Locus T (FT) homologue, underlies a major quantitative trait locus (qDTA8) for flowering time[73]. Interestingly, it has been shown that step-wise cis-regulatory changes occurred in ZCN8 during maize domestication and post-domestication expansion. SNP-1245 is a target of selection during early maize domestication for latitudinal adaptation, and after its fixation, selection of InDel-2339 (most likely introgressed from Zea mays ssp. Mexicana) likely contributed to the spread of maize from tropical to temperate regions[74].

    ZCN8 interacts with the basic leucine zipper transcription factor DLF1 (Delayed flowering 1) to form the florigen activation complex (FAC) in maize. Interestingly, DFL1 was found to underlie qLB7-1, a flowering time QTL identified in a BC2S3 population of maize-teosinte. Moreover, it was shown that DLF1 directly activates ZmMADS4 and ZmMADS67 in the shoot apex to promote floral transition[75]. In addition, ZmMADS69 underlies the flowering time QTL qDTA3-2 and encodes a MADS-box transcription factor. It acts to inhibit the expression of ZmRap2.7, thereby relieving its repression on ZCN8 expression and causing earlier flowering. Population genetic analyses showed that DLF1, ZmMADS67 and ZmMADS69 are all targets of artificial selection and likely contributed to the spread of maize from the tropics to temperate zones[75, 76].

    In addition, a few genes regulating the photoperiod pathway and contributing to the acclimation of maize to higher latitudes in North America have been cloned, including Vgt1, ZmCCT (also named ZmCCT10), ZmCCT9 and ZmELF3.1. Vgt1 was shown to act as a cis-regulatory element of ZmRap2.7, and a MITE TE located ~70 kb upstream of Vgt1 was found to be significantly associated with flowering time and was a major target for selection during the expansion of maize to the temperate and high-latitude regions[7779]. ZmCCT is another major flowering-time QTL and it encodes a CCT-domain protein homologous to rice Ghd7[80]. Its causal variation is a 5122-bp CACTA-like TE inserted ~2.5 kb upstream of ZmCCT10[72, 81]. ZmCCT9 was identified a QTL for days to anthesis (qDTA9). A Harbinger-like TE located ~57 kb upstream of ZmCCT9 showed the most significant association with DTA and thus believed to be the causal variation[82]. Notably, the CATCA-like TE of ZmCCT10 and the Harbinger-like TE of ZmCCT9 are not observed in surveyed teosinte accessions, hinting that they are de novo mutations occurred after the initial domestication of maize[72, 82]. ZmELF3.1 was shown to underlie the flowering time QTL qFT3_218. It was demonstrated that ZmELF3.1 and its homolog ZmELF3.2 can form the maize Evening Complex (EC) through physically interacting with ZmELF4.1/ZmELF4.2, and ZmLUX1/ZmLUX2. Knockout mutants of Zmelf3.1 and Zmelf3.1/3.2 double mutant presented delayed flowering under both long-day and short-day conditions. It was further shown that the maize EC promote flowering through repressing the expression of several known flowering suppressor genes (e.g., ZmCCT9, ZmCCT10, ZmCOL3, ZmPRR37a and ZmPRR73), and consequently alleviating their inhibition on several maize florigen genes (ZCN8, ZCN7 and ZCN12). Insertion of two closely linked retrotransposon elements upstream of the ZmELF3.1 coding region increases the expression of ZmELF3.1, thus promoting flowering[83]. The increase frequencies of the causal TEs in Vgt1, ZmCCT10, ZmCCT9 and ZmELF3.1 in temperate maize compared to tropical maize highlight a critical role of these genes during the spread and adaptation of maize to higher latitudinal temperate regions through promoting flowering under long-day conditions[72,8183].

    In addition, Barnes et al.[84] recently showed that the High Phosphatidyl Choline 1 (HPC1) gene, which encodes a phospholipase A1 enzyme, contributed to the spread of the initially domesticated maize from the warm Mexican southwest to the highlands of Mexico and South America by modulating phosphatidylcholine levels. The Mexicana-derived allele harbors a polymorphism and impaired protein function, leading to accelerated flowering and better fitness in highlands.

    Besides the above characterized QTLs and genes, additional genetic elements likely also contributed to the pre-Columbia spreading of maize. Hufford et al.[85] proposed that incorporation of mexicana alleles into maize may helped the expansion of maize to the highlands of central Mexico based on detection of bi-directional gene flow between maize and Mexicana. This proposal was supported by a recent study showing evidence of introgression for over 10% of the maize genome from the mexicana genome[86]. Consistently, Calfee et al.[87] found that sequences of mexicana ancestry increases in high-elevation maize populations, supporting the notion that introgression from mexicana facilitating adaptation of maize to the highland environment. Moreover, a recent study examined the genome-wide genetic diversity of the Zea genus and showed that dozens of flowering-related genes (such as GI, BAS1 and PRR7) are associated with high-latitude adaptation[88]. These studies together demonstrate unequivocally that introgression of genes from Mexicana and selection of genes in the photoperiod pathway contributed to the spread of maize to the temperate regions.

    The so far cloned genes involved in pre-Columbia spread of maize are summarized in Fig. 2 and Table 2.

    Figure 2.  Genes involved in Pre-Columbia spread of maize to higher latitudes and the temperate regions. The production of world maize in 2020 is presented by the green bar in the map from Ritchie et al. (2023). Ritchie H, Rosado P, and Roser M. 2023. "Agricultural Production". Published online at OurWorldInData.org. Retrieved from: 'https:ourowrldindata.org/agricultural-production' [online Resource].
    Table 2.  Flowering time related genes contributing to Pre-Columbia spread of maize.
    GeneFunctional annotationCausative changeReferences
    ZCN8Florigen proteinSNP-1245 and Indel-2339 in promoter[73, 74]
    DLF1Basic leucine zipper transcription factorUnknown[75]
    ZmMADS69MADS-box transcription factorUnknown[76]
    ZmRap2.7AP2-like transcription factorMITE TE inserted ~70 kb upstream[7779]
    ZmCCTCCT-domain protein5122-bp CACTA-like TE inserted ~2.5 kb upstream[72,81]
    ZmCCT9CCT transcription factorA harbinger-like element at 57 kb upstream[82]
    ZmELF3.1Unknownwo retrotransposons in the promote[84]
    HPC1Phospholipase A1 enzymUnknown[83]
    ZmPRR7UnknownUnknown[88]
    ZmCOL9CO-like-transcription factorUnknown[88]
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    Subsequent to domestication ~9,000 years ago, maize has been continuously subject to human selection during the post-domestication breeding process. Through re-sequencing analysis of 35 improved maize lines, 23 traditional landraces and 17 wild relatives, Hufford et al.[15] identified 484 and 695 selective sweeps during maize domestication and improvement, respectively. Moreover, they found that about a quarter (23%) of domestication sweeps (107) were also selected during improvement, indicating that a substantial portion of the domestication loci underwent continuous selection during post-domestication breeding.

    Genetic improvement of maize culminated in the development of high planting density tolerant hybrid maize to increase grain yield per unit land area[89, 90]. To investigate the key morphological traits that have been selected during modern maize breeding, we recently conducted sequencing and phenotypic analyses of 350 elite maize inbred lines widely used in the US and China over the past few decades. We identified four convergently improved morphological traits related to adapting to increased planting density, i.e., reduced leaf angle, reduced tassel branch number (TBN), reduced relative plant height (EH/PH) and accelerated flowering. Genome-wide Association Study (GWAS) identified a total of 166 loci associated with the four selected traits, and found evidence of convergent increases in allele frequency at putatively favorable alleles for the identified loci. Moreover, genome scan using the cross-population composite likelihood ratio approach (XP-CLR) identified a total of 1,888 selective sweeps during modern maize breeding in the US and China. Gene ontology analysis of the 5,356 genes encompassed in the selective sweeps revealed enrichment of genes related to biosynthesis or signaling processes of auxin and other phytohormones, and in responses to light, biotic and abiotic stresses. This study provides a valuable resource for mining genes regulating morphological and physiological traits underlying adaptation to high-density planting[91].

    In another study, Li et al.[92] identified ZmPGP1 (ABCB1 or Br2) as a selected target gene during maize domestication and genetic improvement. ZmPGP1 is involved in auxin polar transport, and has been shown to have a pleiotropic effect on plant height, stalk diameter, leaf length, leaf angle, root development and yield. Sequence and phenotypic analyses of ZmPGP1 identified SNP1473 as the most significant variant for kernel length and ear grain weight and that the SNP1473T allele is selected during both the domestication and improvement processes. Moreover, the authors identified a rare allele of ZmPGP1 carrying a 241-bp deletion in the last exon, which results in significantly reduced plant height and ear height and increased stalk diameter and erected leaves, yet no negative effect on yield[93], highlighting a potential utility in breeding high-density tolerant maize cultivars.

    Shade avoidance syndrome (SAS) is a set of adaptive responses triggered when plants sense a reduction in the red to far-red light (R:FR) ratio under high planting density conditions, commonly manifested by increased plant height (and thus more prone to lodging), suppressed branching, accelerated flowering and reduced resistance to pathogens and pests[94, 95]. High-density planting could also cause extended anthesis-silking interval (ASI), reduced tassel size and smaller ear, and even barrenness[96, 97]. Thus, breeding of maize cultivars of attenuated SAS is a priority for adaptation to increased planting density.

    Extensive studies have been performed in Arabidopsis to dissect the regulatory mechanism of SAS and this topic has been recently extensively reviewed[98]. We recently showed that a major signaling mechanism regulating SAS in Arabidopsis is the phytochrome-PIFs module regulates the miR156-SPL module-mediated aging pathway[99]. We proposed that in maize there might be a similar phytochrome-PIFs-miR156-SPL regulatory pathway regulating SAS and that the maize SPL genes could be exploited as valuable targets for genetic improvement of plant architecture tailored for high-density planting[100].

    In support of this, it has been shown that the ZmphyBs (ZmphyB1 and ZmphyB2), ZmphyCs (ZmphyC1 and ZmphyC2) and ZmPIFs are involved in regulating SAS in maize[101103]. In addition, earlier studies have shown that as direct targets of miR156s, three homologous SPL transcription factors, UB2, UB3 and TSH4, regulate multiple agronomic traits including vegetative tillering, plant height, tassel branch number and kernel row number[44, 104]. Moreover, it has been shown that ZmphyBs[101, 105] and ZmPIF3.1[91], ZmPIF4.1[102] and TSH4[91] are selective targets during modern maize breeding (Table 3).

    Table 3.  Selective genes underpinning genetic improvement during modern maize breeding.
    GenePhenotypeFunctional annotationSelection typeCausative changeReferences
    ZmPIF3.1Plant heightBasic helix-loop-helix transcription factorIncreased expressionUnknown[91]
    TSH4Tassel branch numberTranscription factorAltered expressionUnknown[91]
    ZmPGP1Plant architectureATP binding cassette transporterAltered expressionA 241 bp deletion in the last exon of ZmPGP1[92, 93]
    PhyB2Light signalPhytochrome BAltered expressionA 10 bp deletion in the translation start site[101]
    ZmPIF4.1Light signalBasic helix-loop-helix transcription factorAltered expressionUnknown[102]
    ZmKOB1Grain yieldGlycotransferase-like proteinProtein functionUnknown[121]
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    In a recent study to dissect the signaling process regulating inflorescence development in response to the shade signal, Kong et al.[106] compared the gene expression changes along the male and female inflorescence development under simulated shade treatments and normal light conditions, and identified a large set of genes that are co-regulated by developmental progression and simulated shade treatments. They found that these co-regulated genes are enriched in plant hormone signaling pathways and transcription factors. By network analyses, they found that UB2, UB3 and TSH4 act as a central regulatory node controlling maize inflorescence development in response to shade signal, and their loss-of-function mutants exhibit reduced sensitivity to simulated shade treatments. This study provides a valuable genetic source for mining and manipulating key shading-responsive genes for improved tassel and ear traits under high density planting conditions.

    Nowadays, global maize production is mostly provided by hybrid maize, which exhibits heterosis (or hybrid vigor) in yields and stress tolerance over open-pollinated varieties[3]. Hybrid maize breeding has gone through several stages, from the 'inbred-hybrid method' stage by Shull[107] and East[108] in the early twentieth century, to the 'double-cross hybrids' stage (1930s−1950s) by Jones[109], and then the 'single-cross hybrids' stage since the 1960s. Since its development, single-cross hybrid was quickly adopted globally due to its superior heterosis and easiness of production[3].

    Single-cross maize hybrids are produced from crossing two unrelated parental inbred lines (female × male) belonging to genetically distinct pools of germplasm, called heterotic groups. Heterotic groups allow better exploitation of heterosis, since inter-group hybrids display a higher level of heterosis than intra-group hybrids. A specific pair of female and male heterotic groups expressing pronounced heterosis is termed as a heterotic pattern[110, 111]. Initially, the parental lines were derived from a limited number of key founder inbred lines and empirically classified into different heterotic groups (such as SSS and NSS)[112]. Over time, they have expanded dramatically, accompanied by formation of new 'heterotic groups' (such as Iodent, PA and PB). Nowadays, Stiff Stalk Synthetics (SSS) and PA are generally used as FHGs (female heterotic groups), while Non Stiff Stalk (NSS), PB and Sipingtou (SPT) are generally used as the MHGs (male heterotic groups) in temperate hybrid maize breeding[113].

    With the development of molecular biology, various molecular markers, ranging from RFLPs, SSRs, and more recently high-density genome-wide SNP data have been utilized to assign newly developed inbred lines into various heterotic groups, and to guide crosses between heterotic pools to produce the most productive hybrids[114116]. Multiple studies with molecular markers have suggested that heterotic groups have diverged genetically over time for better heterosis[117120]. However, there has been a lack of a systematic assessment of the effect and contribution of breeding selection on phenotypic improvement and the underlying genomic changes of FHGs and MHGs for different heterotic patterns on a population scale during modern hybrid maize breeding.

    To systematically assess the phenotypic improvement and the underlying genomic changes of FHGs and MHGs during modern hybrid maize breeding, we recently conducted re-sequencing and phenotypic analyses of 21 agronomic traits for a panel of 1,604 modern elite maize lines[121]. Several interesting observations were made: (1) The MHGs experienced more intensive selection than the FMGs during the progression from era I (before the year 2000) to era II (after the year 2000). Significant changes were observed for 18 out of 21 traits in the MHGs, but only 10 of the 21 traits showed significant changes in the FHGs; (2) The MHGs and FHGs experienced both convergent and divergent selection towards different sets of agronomic traits. Both the MHGs and FHGs experienced a decrease in flowering time and an increase in yield and plant architecture related traits, but three traits potentially related to seed dehydration rate were selected in opposite direction in the MHGs and FHGs. GWAS analysis identified 4,329 genes associated with the 21 traits. Consistent with the observed convergent and divergent changes of different traits, we observed convergent increase for the frequencies of favorable alleles for the convergently selected traits in both the MHGs and FHGs, and anti-directional changes for the frequencies of favorable alleles for the oppositely selected traits. These observations highlight a critical contribution of accumulation of favorable alleles to agronomic trait improvement of the parental lines of both FHGs and MHGs during modern maize breeding.

    Moreover, FST statistics showed increased genetic differentiation between the respective MHGs and FHGs of the US_SS × US_NSS and PA × SPT heterotic patterns from era I to era II. Further, we detected significant positive correlations between the number of accumulated heterozygous superior alleles of the differentiated genes with increased grain yield per plant and better parent heterosis, supporting a role of the differentiated genes in promoting maize heterosis. Further, mutational and overexpressional studies demonstrated a role of ZmKOB1, which encodes a putative glycotransferase, in promoting grain yield[121]. While this study complemented earlier studies on maize domestication and variation maps in maize, a pitfall of this study is that variation is limited to SNP polymorphisms. Further exploitation of more variants (Indels, PAVs, CNVs etc.) in the historical maize panel will greatly deepen our understanding of the impact of artificial selection on the maize genome, and identify valuable new targets for genetic improvement of maize.

    The ever-increasing worldwide population and anticipated climate deterioration pose a great challenge to global food security and call for more effective and precise breeding methods for crops. To accommodate the projected population increase in the next 30 years, it is estimated that cereal production needs to increase at least 70% by 2050 (FAO). As a staple cereal crop, breeding of maize cultivars that are not only high-yielding and with superior quality, but also resilient to environmental stresses, is essential to meet this demand. The recent advances in genome sequencing, genotyping and phenotyping technologies, generation of multi-omics data (including genomic, phenomic, epigenomic, transcriptomic, proteomic, and metabolomic data), creation of novel superior alleles by genome editing, development of more efficient double haploid technologies, integrating with machine learning and artificial intelligence are ushering the transition of maize breeding from the Breeding 3.0 stage (biological breeding) into the Breeding 4.0 stage (intelligent breeding)[122, 123]. However, several major challenges remain to be effectively tackled before such a transition could be implemented. First, most agronomic traits of maize are controlled by numerous small-effect QTL and complex genotype-environment interactions (G × E). Thus, elucidating the contribution of the abundant genetic variation in the maize population to phenotypic plasticity remains a major challenge in the post-genomic era of maize genetics and breeding. Secondly, most maize cultivars cultivated nowadays are hybrids that exhibit superior heterosis than their parental lines. Hybrid maize breeding involves the development of elite inbred lines with high general combining ability (GCA) and specific combining ability (SCA) that allows maximal exploitation of heterosis. Despite much effort to dissect the mechanisms of maize heterosis, the molecular basis of maize heterosis is still a debated topic[124126]. Thirdly, only limited maize germplasm is amenable to genetic manipulation (genetic transformation, genome editing etc.), which significantly hinders the efficiency of genetic improvement. Development of efficient genotype-independent transformation procedure will greatly boost maize functional genomic research and breeding. Noteworthy, the Smart Corn System recently launched by Bayer is promised to revolutionize global corn production in the coming years. At the heart of the new system is short stature hybrid corn (~30%−40% shorter than traditional hybrids), which offers several advantages: sturdier stems and exceptional lodging resistance under higher planting densities (grow 20%−30% more plants per hectare), higher and more stable yield production per unit land area, easier management and application of plant protection products, better use of solar energy, water and other natural resources, and improved greenhouse gas footprint[127]. Indeed, a new age of maize green revolution is yet to come!

    This work was supported by grants from the Key Research and Development Program of Guangdong Province (2022B0202060005), National Natural Science Foundation of China (32130077) and Hainan Yazhou Bay Seed Lab (B21HJ8101). We thank Professors Hai Wang (China Agricultural University) and Jinshun Zhong (South China Agricultural University) for valuable comments and helpful discussion on the manuscript. We apologize to authors whose excellent work could not be cited due to space limitations.

  • The authors declare that they have no conflict of interest. Haiyang Wang is an Editorial Board member of Seed Biology who was blinded from reviewing or making decisions on the manuscript. The article was subject to the journal's standard procedures, with peer-review handled independently of this Editorial Board member and his research groups.

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  • Cite this article

    Biswas O, Kandasamy P, Nanda PK, Biswas S, Lorenzo JM, et al. 2023. Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products. Food Materials Research 3:5 doi: 10.48130/FMR-2023-0005
    Biswas O, Kandasamy P, Nanda PK, Biswas S, Lorenzo JM, et al. 2023. Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products. Food Materials Research 3:5 doi: 10.48130/FMR-2023-0005

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Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products

Food Materials Research  3 Article number: 5  (2023)  |  Cite this article

Abstract: Fish and fish products offer a wide variety of nutritional and health benefits, thanks to the desirable protein and quality. Nevertheless, their quality is prone to degradation due to microbial contamination, oxidation and enzymatic reactions during the storage period. This results in the development of unsuitable flavor and rancid odor hence affecting the freshness, texture and sensory acceptability. Various processing methods such as drying, chilling, freezing etc. are employed, but they seemed to be insufficient to prevent such deterioration. Therefore, additives are added to maintain and/or improve the quality and extend the shelf-life of muscle foods, including fish products. In recent years, natural food additives are well perceived by consumers over synthetic ones. Perceived naturalness is mainly related to healthiness. Natural products, such as plant-derived phytochemicals (phenolics, essential oils, carotenoids, lignins and other molecules), having antioxidant and antimicrobial properties offer plenty of opportunities to overcome protein degradation, lipid peroxidation and also to inhibit microbial growth, thereby improving the quality and shelf-life of food products. This review intends to critically address the potential of phytochemicals as natural food additives to prevent the deterioration of the quality and safety of fish products, and thus providing healthy and safe final products to the consumers.

    • Traditionally, fish is considered an affordable source of protein of high biological value, including high levels of essential amino acids (lysine, methionine, etc.), lipid-soluble vitamins, minerals (Se, P, Fe, Mg, and K), and rich in highly unsaturated fatty acids (ω3, 6, and 9), such as docosahexaenoic and eicosapentaenoic acid[1, 2]. The lipid fraction and other bioactive components present in fish, have attracted a great deal of attention because of their favorable effects on human health[3], including reducing the risk related to human cardiovascular and chronic neurodegenerative diseases. Accordingly, the World Health Organization and American Heart Association have also recommended consuming 1−2 servings of fish weekly regularly. Nevertheless, quality preservation of fish and fish products is challenging due to their high perishability. Further, due to high water and non-protein nitrogen content, the freshness of post-mortem fish muscle rapidly declines. The deterioration in quality of fish due to spoilage by microorganisms[4]. Further microbial spoilage leads to lipid oxidation resulting deterioration of different quality aspects of fish. In general, fish spoilage is governed by three basic mechanisms namely enzymatic autolysis, microbial growth and lipid peroxidation. All three, in a favourable condition continue simultaneously in a food substrate and after a certain interval, the evidence of spoilage could be noticed.

      Spoilage is considered as one of the major concerns of fish food safety which may cause several negative effects on the health of the consumers. For this reason, commonly, one or more preservation technique(s) is employed to extend their shelf life, with the purpose to prevent and or delay quality changes[5]. Traditional preservation methods, including drying by different means such as salting, smoking, fermentation, etc., low-temperature storage (chilling, freezing), or with chemical preservatives, have been commonly used in the industry. Nowadays, non-thermal physical technologies (pulsed electric fields-PEF, high hydrostatic pressure-HPP, ionizing radiation ultrasonication, cold plasma, and innovative packaging systems) are also being employed for the same purposes[6]. Likewise, PEF and HHP treatments may not ensure food safety, as these can only cause sublethal damage to the bacterial cell wall[7]. Beside processing strategies, various organic acids and their different salts (such as sorbic acid, benzoic acid, propionic acid, sodium benzoates, propionates, potassium sorbates, nitrites, ascorbic acid, citric acid, etc.), and synthetic phenolic compounds such as butylated hydroxyl toluene (BHT), butylated hydroxyl anisole (BHA), tert-butylated hydroquinone (TBHQ), dodecyl gallate are used as food preservatives[8]. Incorporating synthetic antioxidants viz., BHT, BHA, TBHQ at high doses, either to the raw materials or end-products can negatively affect human health[9]. Prolonged use of these synthetic preservatives and compounds are reported to induce cancer, liver and kidney damage, gastrointestinal disorders, asthma, and many allergies[10].

      With increased concerns and negative perceptions among consumers regarding the safety aspects of chemical preservatives and synthetic compounds, the demand for minimally processed ready-to-eat fish products has increased many-fold. To cater to the demand of consumers and to ensure the availability of safe, nutritious, tasty, and convenient food, natural alternatives, such as those involving phytochemicals/phytoextracts, including essential oils, phenolics etc. derived from plants have gained lots of interest. Plants and their parts harbor a complex mixture of bioactive compounds that are a good source of phytochemicals such as polyphenols, phytosterols, alkaloids, nitrogen-containing compounds, terpenoids, organosulfur compounds etc. These compounds possess inherent biological effects such as antimicrobial, antioxidant, antidiabetic, anti-inflammatory, immune-enhancing functions etc. that are reported to offer health benefits[1113] and form the major basis of Ayurveda, Unani, Siddha and the Chinese system of medicine since antiquity.

      As the focus of the processing industry is to maintain the organoleptic and nutritional characteristics and ensure the quality and safety of food products, the phytoextracts/phytochemicals derived from plants are gaining increasing importance nowadays. This paper aims to provide an overview of the recent applications of phytoextracts/phytochemicals for shelf-life extension and nutritional and organoleptic quality and sensory improvement of the fish, and its products.

    • Phytochemicals, also called green chemicals, produced by plants through primary or secondary metabolism, are gaining attraction as healthier alternatives to synthetic antioxidants and antimicrobials[14]. The phytochemicals are extracted from various plant parts (leaves, shrubs, seeds, flowers, fruits, bark etc.). They also can be recovered from the residues and leftovers of fruits and vegetables (peels, pulp) generated during harvesting and processing[15] and thus contribute to waste valorization and circular economy[11]. Generally, based on their chemical structure and characteristics, the secondary metabolic products of plants are classified into phenolics, terpenoids, carbohydrates, phytosterols, alkaloids and other nitrogen-containing compounds[1113]. Phenolics are the largest category of phytochemicals being structurally diverse and abundantly distributed in the plant kingdom. They can be divided into phenolic acids (hydroxybenzoic acids − e.g. gallic, ellagic, vanillic acids etc.; hydroxycinnamic acids − e.g. caffeic, chlorogenic, cinnamic, ferulic etc.), flavonoids (flavones, flavonols, flavan-3-ols, isoflavones, anthocyanidins, anthocyanins etc.) and other phenolics (tannins, stilbenes, lignans, xanthones, lignins, chromones etc.)[16]. Among flavonoids, flavonols like quercetic, rutin, myricetin, kaempferol etc. and flavon-3-ols like catechin, epicatechin etc. are common. Apart from flavonols and flavones, anthocyanins and anthocyanidins are major flavonoids widely available in various fruits and vegetables such as grapes, apples, plums, cabbage, purple corn, and different varieties of berries like elderberry, blueberry, blackberry, elderberry, etc. Popular bioactive compounds among anthocyanins and anthocyanidins are cyanidin, malvidin, delphinidin, peonidin, petunidin, pelargonidin, etc.[11].

      Terpenes, also known as terpenoids, exhibit diverse biological and pharmacological properties which are beneficial to humans. Based on the number of C5 isoprene unit, terpenes are grouped as hemiterpenes (prenol and isovaleric acid), monoterpenes (geraniol and limonene), sesquiterpenes (farnesol), diterpenes (quinogolides and taxadiene), sesterterpenes, triterpenes (squalene), tetraterpenes and ployterpenes[17]. Carotenoids such as lycopene, phytoene, phytofluene, lutein, zeaxanthin, β-cryptoxanthin, astaxanthin etc. are tetraterpenes reported to have many biological functions. These terpenoids form the major constituents of various essential oils.

      Essential oils (EOs) obtained from various parts of plants (leaves, barks, stems, roots, flowers, and fruits) are complex mixtures of numerous individual aromatic volatile compounds that can act as defense mechanisms against microorganisms[18]. These volatile compounds belong to various chemical classes: alcohols, ethers or oxides, aldehydes, ketones, esters, amines, amides, phenols, heterocycles, and mainly the terpenes. Thousands of compounds belonging to the family of terpenes have so far been characterized and identified in essential oils[19], such as functionalized derivatives of alcohols (α-bisabolol), ketones (menthone, p-vetivone) aldehydes (citronellal, sinensal), esters (γ-tepinyl acetate, cedryl acetate), and phenols (thymol). Interestingly, EOs also contain non-terpenic compounds which are bio-generated by the phenylpropanoids pathway, like eugenol, cinnamaldehyde, and safrole[20]. Figure 1 illustrates the different kinds of natural bioactive compounds extracted from various plant components.

      Figure 1. 

      Schematic diagram of different components in phytochemicals.

    • After harvest, different activities namely oxidative and enzymatic autolysis in fish cause deteriorative changes in sensory and nutritional value. These changes not only cause the loss of freshness as perceived by consumers but also limit the shelf-life during storage. Again above deteriorative changes with loss of freshness are mainly due to lipid oxidative products and protein degradation, which accelerate the undesirable changes in color, flavor and texture in fish. A wide range of plant extracts rich in polyphenols have been used for the preservation of fish and fish products, because of their antioxidant and antimicrobial activities. These extracts are applied either as dip treatment or as a coating in raw, chilled, and frozen stored products[21]. Various packaging methods viz. vacuum packaging and modified atmospheric packaging (MAP) are employed for extending the shelf life during the storage and retailing of fish and fish products. Different plant extracts are also being incorporated into ice to enhance the quality attributes of fish during storage[22]. In a recent study, the application of oregano essential oil (OEO) vapors under vacuum conditions, immediately before packaging, has been reported to be more effective than conventional dipping and topical application in maintaining the freshness and quality of fish products[23]. The effect of various phytochemicals on the quality aspects of fish and fish products is depicted in a schematic diagram shown in Fig. 2.

      Figure 2. 

      Schematic diagram showing the effect of various phytochemicals on quality aspects of fish and fish products.

    • Physicochemical properties like pH, water holding capacity, emulsion stability, cooking yield, etc., play important roles in case of emulsion-based muscle foods, including fish products. Amongst these, pH and water holding capacity are regarded as critical quality parameters in muscle food products due to their closest adherence to texture, cooking loss, juiciness, tenderness, and microbial quality of the products. Several reports on phytoextracts and their effects on the pH, water holding capacity, yield, total volatile basic nitrogen (TVB-N), trimethylamine (TMA-N) etc. of fish and fish-based products are available in the literature (Table 1).

      Table 1.  Effect of phytochemicals as bioactive compounds on physicochemical, microbiological and sensory quality of fish and fish products.

      Fish and fish productsPhytochemical usedParameters studied Key findingsReferences
      Salted sardines
      (Sardina pilchardus)
      Lemon essential oil (EO) micro-emulsion at 3 and 10 g/kgChemical, microbiological and sensory parameters of salted sardines during the entire period of ripening (150 d)• Retarded the growth of Enterobacteriaceae by 0.95 CFU/g, Staphylococci by 0.59 CFU/g, and rod lactic acid bacteria by 1.5 log cycles
      • Lowered the accumulation of histamine
      • Registered highest scores for flavor and overall acceptability
      [46]
      Common carp (Cyprinus carpio) filletsCinnamon essential oil (1 g/kg)Physicochemical, spoilage microbes and sensory attributes of fillets stored at 4 ± 1 °C for 14 d• Decreased the relative abundance of Macrococcus (51.8% vs 33.4%)
      • Effective in inhibiting the increase of TVB-N and the accumulation of biogenic amines.
      • Extended the shelf life of vacuum-packed fillets
      [40]
      Fillets of Sardinella longiceps and Rastrelliger kanagurtaColeus aromaticus and Sargassum wightii leaf pasteProximate, microbiological, and sensory characters of fillets under chilled storage (4 ± 1ºC) conditions for 7 d• Significantly (P ˂ 0.05) improved proximate parameters with reduced moisture and TVC content as compared to control
      • Treated fillets had the best appearance, smell, color, texture, and taste compared to control
      S. wightii proved to be a better preservative than C. aromaticus
      [27]
      Smoked tilapia
      (Oreochromis niloticus) fish
      Ginger, garlic and clove powder
      (5 g/kg)
      Microbial activity, shelf life and safety of fish during 8 weeks of storage• Preservatives treated samples had reduced microbial load, and longer shelf-life (8 weeks)
      • Treated samples recorded zero/no total coliform count (TCC) growth and were accepted by the consumers
      [47]
      Frozen rainbow trout filletsClove oil (5 and 10 g/kg) used as natural preservative
      Microbiological and sensory quality of frozen and vacuum-packed rainbow trout fillets stored at -18 °C for six months
      • Microbial growth was high for frozen storage for control samples
      • Samples with clove oil had longer shelf life than normal
      • Clove oil can be used as a natural protective and influential antibacterial in conjunction with a vacuum pack to augment the quality
      [64]
      Founder (Paralichthys orbignyanus) filletsFillets packed in agar film with fish protein hydrolysate
      (FPH) (500g FPH/ kg agar) or with film containing clove EO (500 g EO/kg agar)
      Microbiological quality and shelf life of fillets stored at 5 °C for 15 d• Fillets packaged with film containing clove EO had better microbiological quality than packaged in agar film with FPH
      • Both the films effective in extending the shelf-life of fillets
      [65]
      Fish surimi from
      O. niloticus
      Treating of surimi gel by immersion with colored plant extracts- CPEs
      (2.5 g/L)- Hibiscus sabdariffa calyces, Curcuma longa rhizomes, and Rhus coriaria fruits
      Microbiological and sensory attributes of samples aseptically packaged into polyethylene bags and stored at 4 °C for 7 d
      H. sabdariffa extract was the most effective antimicrobial
      • CPEs enhanced sensorial attributes of surimi during storage study
      • CPEs application as colorants and antibacterial and quality enhancing agents recommended for biopreservation of seafood
      [54]
      Fish patties from Hake fillets (Merluccius capensis, Merluccius paradoxus)Extract from pomegranate peel, rosemary, citric, and hydroxytyrosol (obtained from vegetable waters of olive tree)
      (@ 0.2 g/kg)
      Physicochemical, microbiological properties, sensory analysis, and shelf life of patties under chilled storage for 14 d• Patties with rosemary extract had a high level of protein (140 g/kg),
      α-linolenic acid (up to 400 g/kg), selenium minerals, and low fat
      (< 20 g/kg) compared to the control
      • Extracts effective against protein oxidation of patties than commercial preservatives added to the control
      • Patties with pomegranate extract had a longer life (7 to 11 d) than others (4–6 d)
      [28]
      Grass carp (Ctenopharyngodon idellus) filletsTreatment with essential oils (EOs)- oregano (Origanum vulgare), thyme (Thymus mongolicus Ronn.), and star anise (Illicium verum) @ 1 g/L for 30 min at room temperatureMicrobial composition and quality of fillets stored at 4 ± 1 °C• EOs effective in inhibiting microbial growth (TVC) by 0.59 log CFU/g, delaying lipid oxidation, and retarding the increase of TVB-N, putrescine, hypoxanthine, and K-value
      • Samples with EOs had a less fishy smell and firmer texture compared to the control
      • EOs extended the shelf-life of fillets by 2 more days compared to the control
      • Treatment with EOs can effectively inhibit the degradation of ATP and maintain a high quality of fish products
      [4]
      Sea bream (Sparus aurata) fresh filletsApplication of oregano essential oil (OEO) in the vapor phase (67 µL/L) under vacuum (5–10 hPa) immediately before MAP fillet packagingMicrobial and sensory product quality of fish fillets stored at 4 ºC for 28 d• OEO vapor treated samples had better physicochemical parameters (pH, TMA-N and WHC) as well as freshness compared to dipping
      • Shelf life of vapor OEO treated MAP fish fillets was extended up to 28 d compared to control (7 d)
      • Microbial quality of fish fillets is well preserved with the innovative OEO vapor injection under vacuum
      [23]
      Sardine (Sardinella albella) muscleBetel leaf (Piper betle) extracts (BLE)
      @ 0.5 and 1 g/kg in the ice medium
      Microbial, biochemical, and sensory score of fish during 14 d of chilled storage• BLE at both concentrations inhibited the microbial proliferation and fish deterioration and extended the shelf life of fish for at least 3 d compared to the control sample
      • BLE incorporated into ice improved the sensory score and chemical (pH, TVB-N, and TMA-N) quality
      [30]
      Indian mackerel (R. kanagurta)Methanolic extract of the red alga Gracilaria verrucose-GC @ (0.67 and 2.5 g lyophilized alga/L aqueous solution) in the icing mediumMicrobial, chemical, and sensory study of fish chill stored for 15 days• GC significantly (P < 0.05) inhibited the mesophilic and psychrophilic bacteria and chemical markers (pH, TVB-N, TMA-N, and biogenic amines) of fish deterioration relative to the control
      • Icing medium containing GC extract improved the sensory acceptability, quality, and safety of fish compared to control
      • The seafood industry can explore icing medium containing GC as a biopreservative
      [66]
      Hairtail fish ballAqueous solution containing 1 g/kg sage extract, 1 g/kg oregano extract and
      0.1 g/L grape seed extract (GSE)
      Quality and volatile flavor component of
      fish balls stored at 4 °C up to 15 d
      • GSE stabilized meatball pH of hairtail fish
      • The extract also reduced fishy odor, TBARS values, and TVB-N
      • Inhibited bacterial growth compared to control
      [67]
      Wallago attu fish nuggetsTreated with guava (Psidium guajava L.), bael (Aegle marmelos L.) pulp and dragon fruit (Hylocereus undatus L.) peel powder @ 15 g/kgVarious physicochemical,
      textural and sensory attributes of fish nuggets refrigerated stored up to 10 d
      • Fruits powder @ 15 g/kg significantly reduced the pH of the nuggets compared to control
      • Increased emulsion stability, cooking yield, moisture, fat, and protein percentage
      • Slowed down the lipid peroxidation of fish nuggets
      • Textural attributes were improved in treated nuggets
      [25]
      Minced meat of Indian mackerel (R. kanagurta)Pomegranate peel extract (PPE)
      @ 1, 1.5, and 2 g/kg
      Oxidative stability of samples packed in polythene bags and stored at 4 °C• PEE @ 2 g/kg ppm increased oxidative stability of minced meat
      • Improved shelf life of fish meat up to 8 days compared to 4 d in control
      [41]
      Canned common barbel (Barbus barbus) fish burgersCystoseira compressa and Jania adhaerens powder @ 5, 10, and
      15 g/kg
      Texture and sensory characteristics of fish burgers stored at 4 ºC for further analyses (8 months)• Treated formulations had improved nutritional content WHC, and enhanced texture stability
      • Burgers containing 10 g/kg algae had better texture and sensory properties (P < 0.05)
      • Algae could be considered as nutritious additives and natural flavoring and coloring agents to produce fish-based products
      [68]
      Cobia (Rachycentron canadum) filletsPsidium guajava extract (PGE)
      @ 0.3 g/kg (w/v) for 30 min
      Physicochemical and microbiological changes in fillets packed and stored in ice for 15 d• PGE @ 0.3 g/kg showed a significantly lower increment of pH values during storage
      • Treated fillets showed significantly higher sensory properties, lower PV and TBARs compared to the control
      [24]
      Bighead carp (Aristichthys nobilis) filletsAqueous pomegranate peel extract (APPE) @ 0.5 g GAE/L and ethanolic pomegranate peel extract (EPPE)
      @ 0.5 g GAE/L
      Microbiological and quality changes in fillets stored at 4 °C for 8 d• PPE decreased the TVC of fish spoilage bacteria such as Pseudomonas, Aeromonas, and Shewanella
      • APPE is more effective in retarding the
      increase of TVB-N and K-value
      • EPPE was relatively better in inhibiting biogenic amines
      [52]
      Atlantic mackerel (Scomber scombrus) filletsFillets immersed in 10 g/L of rosemary or basil essential oils (EOs) for 30 min at 2 °CPhysicochemical quality of fillets stored at 2 °C up to 15 d• Rosemary and basil treatments effectively inhibit the formation of TVB-N and lipid oxidation products during storage.
      • Significantly lower pH values were observed for the basil group than others, indicating antimicrobial effects
      • Compared to the control group, fillets treated with rosemary and basil EOs had extended shelf life by 2 and 5 d
      [69]
      Common Carp (C. carpio) filletsEdible coating (C + EC), edible coating +, 5 g/kg chitosan (C + ECCh) and edible coating + 15 g/kg chitosan + 100 g/kg peppermint (C + ECChP)Quality and shelf life of common carp (C. carpio) during refrigerated storage (4 ± 1 °C) for 9 d• ECChP coating treatment extended the shelf life of carp by about 4 days compared with the control
      • (C + ECCh) and (C + ECChP) significantly effective (P < 0.05) in delaying hydroperoxide production of fillets during refrigerated storage, reducing lipid oxidation
      [36]
      Fish (S. scombrus) minceGreen tea
      extract (GTE), grape seed extract (GSE), and pomegranate rind extract (PRE) at a level of 0.1 g/kg equivalent phenolics
      Changes in quality of fish mince during frozen storage at −18 ± 1 °C for 6 months
      • PRE effectively inhibited lipid oxidation with lower peroxide and TBARS values
      • Minced fish containing PRE had lower carbonyl and higher sulfhydryl contents
      • GTE was not effective against lipid and protein oxidation
      • PRE could be utilized as an antioxidant to extend the storage period in raw minced fish tissue
      [34]
      Fried fillets of Nile tilapia (O. niloticus)Fillets treated with rosemary extract-RE (1, 2, 3 g/kg) and Vitamin E 1 g/kgPhysicochemical and sensory quality of fried fillets stored for 15 d at
      4 ± 1 °C and 3 months at −18 ± 2 °C
      • TMA-N and TVB-N, values of RE and vitamin E treated samples were significantly lower than control samples (P < 0.05)
      • R.E. @ 3 g/kg retarded oxidative changes in chilling and frozen fried fillets
      • Significant (P < 0.05) enhancement in sensory quality attributes in samples treated with RE and vitamin E
      [59]
      Whole rainbow trout (Oncorhynchus mykiss)Effect of ice coverage comprised of Reshgak (Ducrosia anethifolia) extract (RE) @ 3 mg/L and Reshgak essential oil (REO) @ 15 g/LChemical, microbiological and shelf life study during a 20-day storage period.• Treated samples had lower bacterial counts and chemical indices than ice coverage without extract
      • Fish stored in ice containing REO had a longer shelf-life (> 16 d) than RE (16 d) and lot stored in traditional ice (12 d)
      [70]
      TMA-N = Trimethylamine; TVB-N = Total volatile basic nitrogen; TVC = Total viable count; TBARS = Thiobarbituric acid reactive substances; WHC = Water holding capacity; MAP = Modified atmosphere packaging.

      The cobia (Rachycentron canadum) fish fillets treated with guava leaf extract had significantly lower pH values than the control samples during storage for up to 15 d[24]. Likewise, the incorporation of different fruit powders viz. guava and bael pulp at 15 g/kg were found to significantly reduce the pH of fish nuggets[25]. The application of oregano EO in the vapor phase (67 μL/L) under vacuum (5−10 hPa) immediately before MAP of sea bream (Sparus aurata) fresh fillets has also been reported to maintain the physicochemical parameters like pH, TMA-N, water holding capacity and freshness[23]. The lower pH, TMA-N and freshness in treated fillets might be due to inhibition of spoilage microorganisms by EO vapors and reduced accumulation of alkaline compounds from protein degradation and decarboxylation of amino acids. Furthermore, the acidic nature and ascorbic acid content of plant extracts applied in powder form contributed to lowering the pH of fish products.

      Sardine (Sardinella aurita) fillets marinated with pomegranate (Punica granatum L.) peel and artichoke (Cynara cardunculus L.) leaves extracts had the lowest pH value, TVB-N, and histamine content at the end of the storage time, resulting in less microbial spoilage compared to the control group[26]. In another study, the Coleus aromaticus leaf and microalga (Sargassum wightii) paste significantly improved protein, lipid, and carbohydrate contents while reducing moisture content of fish fillets of Sardinella longiceps and Rastrelliger kanagurta stored under chilled conditions for 7 d compared to control[27]. Apart from exhibiting antioxidative and antimicrobial activities, phytoextracts also preserved/improved the nutritional value of products. For example, fish patties incorporated with rosemary extract at 0.2 g/kg were found to have higher protein (140 g/kg), phosphorus and selenium minerals, alpha-linoleic acids up to 400 g/kg and low-fat contents (< 20 g/kg), compared to the control sample[28].

      Fish nuggets with dragon fruit peel powder (10, 15 and 20 g/kg) have been reported with lower pH values, and significantly improved emulsion stability and cooking yield compared to the control[29]. This might be due to the water and fat-binding properties of dietary fibre present in dragon fruit peel powder. Betel leaf (Piper betle) extracts (0.5 and 1 g/kg) in ice medium have also been reported to improve the chemical quality such as pH, TVB-N, TMA-N and extend the shelf life of sardine muscle[30]. Essential oils like oregano, thyme, and star anise (1 g/L) were reported to be effective in delaying lipid oxidation, biogenic amines formation and TVB-N putrescine, and hypoxanthine of grass carp fillets. Besides, these EOs also delay the degradation of ATP and IMP which in turn helps in maintaining the quality of fish products[4].

    • Fish oils contain unsaturated fatty acids, especially polyunsaturated fatty acids (PUFA) which are easily susceptible to oxidative changes. Hence fish and fish products are preserved for longer periods of time with additives having antioxidant properties. During the storage of food products, peroxide value (PV) and thiobarbituric acid (TBA) are considered useful indicators to determine the degree of lipid oxidation. In a study conducted by Mazandrani et al.[31], the peroxide and TBA values of silver carp fillets treated with liposomal encapsulated fennel extracts were significantly lower than the control during storage, suggesting that the fennel extract after encapsulation in liposome may be more effective in lowering lipid oxidation. The preservative effect of dried red beetroot peel (DRBP) extract was studied to monitor the quality changes, such as TBA and sensory values in Nile tilapia fish fillet. The fillets treated with DRBP extract at 1 g/L had reduced TBA content and acceptable sensory scores compared to non-treated samples[32]. The antioxidant potential of the peel extract primarily could be due to the presence of betaines, phenolic and flavonoid compounds containing amino and hydroxyl groups, and other active components such as carotenoids and glycine. In another study, aqueous extracts of seaweed (Padina tetrastromatica) applied at 2% as an additive has been reported to reduce the meat discoloration and fat oxidation in Pangasius fish fillets, and thus extending their storage life[33]. This could be due to tannic acids in seaweed extracts which reduced the myoglobin oxidation resulting in higher redness values. Pomegranate rind extract (PRE) at 0.1 g/kg equivalent phenolics was also reported to significantly reduce lipid oxidation (with lower peroxide and thiobarbituric acid reactive substances, TABRS) and protein oxidation (with lower carbonyl and higher sulfhydryl contents of fish mince during frozen storage)[34]. Protein oxidation can be assessed continuously by analyzing the carbonyl and sulfhydryl contents to understand the extent of protein damage during storage[35].

      Edible coating of chitosan and peppermint has been reported to extend the shelf life of common carp (Cyprinus carpio) fillets during refrigerated storage, by delaying the hydroperoxide production, and also by reducing lipid oxidation[36]. The reduction of lipid oxidative products or delaying hydroperoxide production could be due to antioxidants present in chitosan and peppermint coating by quenching fatty acids or hydroxy radicals. In another study, basil leaf extract (10 g/L) was effective in inhibiting the formation of TVB-N and other lipid oxidative products in fillets of Atlantic mackerel (Scomber scombrus) during storage. Again, basil leaf essential oil combined with ZnO nanoparticles significantly lowered the production of TVB-N, biogenic amines, peroxide, and TBARS values during storage of sea bass (Lates calcarifer) slices[37]. The lower production of TVB-N in treated sample could either be due to the rapid inhibitory effect of bacterial growth or decreased bacterial capacity for oxidative de-amination of non-protein nitrogenous compounds, or both especially by basil leaf EO-ZnO nanoparticles film. Recently, hemp essential oil reinforced in nanoparticles with whey and mung bean proteins complex has been reported to inhibit the microbial activity, lipid oxidation and TVB-N in rainbow trout fillets during refrigerated storage[38]. Nisin and EO from Mentha pulegium. L. when used in free and nanoliposome forms minimized the growth of spoilage microorganisms, TVB-N production and improved sensory properties of minced fish[39]. In the aforesaid studies, amino acid decarboxylase inhibiting properties of EOs might be the reason for the low levels of TVB-N and biogenic amines in treated fish products during storage[40]. Pal et al.[41] reported the presence of high content of phenolic compounds like punicalagin, punicalin, gallic acid, and ellagic acid in pomegranate peel extract (PPE) which extended the shelf life of Indian mackerel mince (by up to 8 d). This could be due to higher antioxidant activity of ethanolic extract of pomegranate peel, when used at a concentration of 2 g/kg as compared to control.

      Betel leaf extract in ice medium has been reported to significantly extend the shelf life of sardine muscle by reducing the production of TVB-N and TMA-N during storage[30]. Recently, extracts from various fruits such as blueberry, acerola, and grape have significantly inhibited the formation of heterocyclic aromatic amines (HAAs) in roasted yellow croaker. Particularly, blueberry extract was more effective in reducing the Norharman (94.85%) and heterocyclic amine 2-amino-1-methyl-6-phenylimidazo[4-5-b]pyridine (PhIP) (71.15%) content compared to fruit extracts[42]. Different fruits extracts possibly hindered the pyridines and pyrazines via Strecker degradation, derived from various precursors, including amino acids and glucose, responsible for formation of HAAs[43]. Interestingly, the use of herbs such as parsley (40 g/kg), chives (40 g/kg), and their mixture (Brazilian cheiro-verde) effectively inhibited the formation of cholesterol oxidation products (COPs) in grilled sardine fish[44]. As the formation of higher PhIP content in cooked muscle foods is considered mutagenic and carcinogenic, natural extracts from plant components could be an effective approach to minimize the formation of HAAs in muscle food products.

    • Available reports suggest that essential oils from plants, when applied as natural preservatives, show good antimicrobial activity, and maintain the quality of fish and fish products during storage. Antimicrobial effect of EOs is mainly due to interaction of hydrophobic part oil with lipid components of cell membrane of the bacteria resulting in change in sequences of metabolic function and cell death[45]. The addition of lemon EO micro-emulsions retarded the growth of Enterobacteriaceae, Staphylococci, and rod-shaped lactic acid bacteria in salted sardines[46]. Likewise, hot smoked tilapia (Oreochromis niloticus) treated using EOs (extracts of ginger, garlic, clove) had significantly lower total viable, total psychotropic, lactic acid bacteria count for 7 weeks storage period[47]. The inhibitory effects of olive by-products (such as olive leaf extract-OL, olive cake-OC, and black water-BW) were studied on fish spoilage bacteria from anchovy, mackerel, and sardine. Kuley et al.[48] reported that OL extract was more sensitive to fish spoilage bacteria and reference strains such as Enterobacter cloacae, Serratia liquefaciens, Proteus mirabilis, Photobacterium damseale, Pseudomonas luteola, Pantoea spp., Vibrio vulnificus, Stenotrophomonas maltophila, Acinetobacter lwoffii, Pasteurella spp., and Citrobacter spp. The effect of salep gum containing orange peel essential oil (2.5 and 5 g/kg) coating on the microbial growth and shelf life of rainbow trout (O. mykiss) fish fillets stored for 16 d under refrigerated conditions was investigated[49]. Samples treated with 5g/kg orange essential oil had improved shelf life and low numbers of total aerobic mesophilic, psychrophilic, coliforms and lactic acid bacteria, which can be ascribed to the presence of antimicrobial compounds (limonene and other minor compounds) in orange essential oil, exhibiting antimicrobial effects.

      The EO of Zataria multiflora Boiss (ZMB) was reported to be more sensitive, particularly to Gram-negative more than Gram-positive bacteria that cause seafood spoilage, hence can be used as a natural additive for food preservation[50]. However, Hosseini et al.[51] indicated that the highest concentration with sensory acceptability of ZMB EOs when used in rainbow trout cannot inhibit the growth of L. monocytogenes at room, and optimum growth temperature. The variation in antibacterial effect of EOs may be due to factors such as the type, concentration, and form of EOs (liquid or vapor), number of microorganisms and influence of food matrix such as low pH value, level of sodium chloride etc. The vapor phase of various EOs has also been reported to have antimicrobial activity in various food systems. In a recent study, the vapor phase of oregano EO under vacuum immediately before MAP packaging has been reported to limit the microbial growth and maintain the quality of sea bream fresh fillets during refrigerated storage for 28 d. Chemically, the vapor phase of EOs being hydrophobic in nature are accumulated in the lipid component of microbial cell membrane hampering its functional properties, thus leading to structural damage[23].

      Various researchers have reported the antimicrobial effect of pomegranate peel extract (PPE) on the quality and shelf life of fish and fish products, mainly due to the presence of higher phenolic components such as punicalagin, gallic acid, ellagic acid, chlorogenic acid, caffeic acid, catechin, epicatechin, rutin, quercetin, and galangal[26]. Zhuang et al.[52] reported that bighead carp (Aristichthys nobilis) fillets treated with PPE at 0.5 g GAE/L had significantly decreased total volatile compounds (TVC) of fish spoilage bacteria such as Pseudomonas, Aeromonas, and Shewanella, during chilled storage. The efficacy of pomegranate peel powder breaded on ready-to-cook cod sticks was studied against total mesophilic, psychrotrophic and other spoiling bacteria, Pseudomonas spp., Shewanella putrefaciens and Photobacterium phosphoreum[53]. The study reported a delayed microbial growth in treated samples stored for 17 d under refrigerated conditions, which could be due to higher bioactive compounds such as polyphenols, tannins, flavonoids and anthocyanins in peel powder, exhibiting antibacterial activity. Even colorants obtained from plant extracts such as Hibiscus sabdariffa calyces, Curcuma longa rhizomes, and Rhus coriaria fruits are reported to exert an antimicrobial effect on standard microbial stains like Escherichia coli (ATCC 25922), Salmonella typhimurium (ATCC 14028), Staphylococcus aureus (ATCC 25923), and Pseudomonas aeruginosa (ATCC 27853) in surimi from O. niloticus[54]. Dip treatment of Deccan mahseer (Tor khudree) steaks with beetroot (Beta vulgaris) peel extract (200 g/L) has been reported to exhibit a positive effect by retarding spoilage, thereby extending shelf life up to six months during frozen storage study[55]. The addition of Simira ecuadorensis plant extract (80 g/kg) significantly reduced the aerobic mesophilic bacteria count in a fish burger[56]. The extract reduced the pH of fish burger thereby increased the microbiological safety during further storage periods. Betel leaf extract has also been reported to significantly lower microbial proliferation and prolongs the shelf life of sardine muscle for at least 3 more days compared to the control[30]. In a similar study, the fillets of O. niloticus treated with ethanolic extracts of betel leaf at 0.4 and 0.6 g/kg had reduced microbial growth and quality deterioration during 12 d of storage at refrigerated temperature, compared to untreated samples[57]. The minimum inhibitory concentration (MIC) of various phytochemicals against different fish spoilage microorganisms is presented in Table 2.

      Table 2.  Minimum inhibitory concentration (MIC) of phytochemicals against fish spoilage microorganisms.

      Component of plantsFish productsMIC values Target microorganismsReferences
      Curcuma longa rhizome powder (200 g/L of 70 % aqueous ethanolic solution)
      Surimi gel of tilapia2.2 g/L
      1.8 g/L
      1.8 g/L
      1.2 g/L
      Salmonella Typhimurium
      Staphylococcus aureus
      Escherichia coli
      Pseudomonas aeruginosa
      [54]
      Gabsi pomegranate peel powder (5 g powder in
      150 mL methanol for methanol pomegranate peel extracts)
      fresh fish152 g/LE. coli
      Saccharomyces cerevisiae
      [71]
      Olive leaf extract (OL), olive cake (OC), black
      water (BW)
      Fresh anchovy, mackerel, sardine3.0 g/L
      6.0 g/L
      12.5 g/L
      E. coli
      Salmonella Paratyphi A
      S. aureus
      [48]
      Betel leaf (Piper betle) powder (water extract)Sardine fish meat0.5 g/LPsychrophilic bacterial count[30]
      Hibiscus sabdariffa
      Calyces powder (200 g/L of 70% aqueous ethanolic solution)
      Surimi gel of tilapia1.6 g/L
      1.0 g/L
      1.2 g/L
      1.6 g/L
      S. Typhimurium
      S. aureus
      E. coli
      P. aeruginosa
      [54]
      Thyme essential oilMinced fish meat8 g/kgListeria monocytogenes[72]
      Lavender essential oilCatfish2 g/L,
      1–1.2 g/L
      E. coli,
      S. aureus
      [73]
      Kakadu plum bark powder (methanol extract)
      Chilled fish1 g/LS. aureus[74]
      Fruits and culinary herbs of Australian plant powder (methanolic extract)Fresh fish5 g/LShewanella putrefaciens[75]
      Dried, fragmented leaves of rosemary, thyme and
      dried fruits of anise (Pimpinella anisum)
      Canned fish10 g/L (rosemary)
      1.25 g/L (thyme)
      10 g/L (anise)
      Clostridium perfringens[76]
      Simira ecuadorensis leaf powder (ethanol extract)Fish hamburger80 g/LCampylobacter jejuni
      and S. putrefaciens
      [56]
    • The use of phytochemicals in extract, powder, or oil forms influences the sensory attributes of fish and fish products at different levels of efficiency. Fish paste (pollack meat, cuttlefish meat, shrimp meat) received the best score in terms of taste and overall preference, when treated with different levels (10, 30, 50, and 70 g/kg) of C. longa powder[58]. Fish nuggets treated with dragon peel powder at 15g/kg had improved shelf life and sensory attributes compared to others during 15 d of storage[29]. Fillets of S. longiceps and R. kanagurta treated with leaf paste of C. aromaticus and S. wightii had the best appearance, smell, color, texture, and taste compared to control[27]. Even ethanolic extracts of betel leaf at 0.4 or 0.6 g/kg has been found to extend shelf life without any change in taste or discoloration of Nile tilapia (O. niloticus) fillets up to 9 d[57]. In a recent study, fried fillets of Nile tilapia (O. niloticus) treated with rosemary extract (1, 2, 3 g/kg) and vitamin E (1 g/kg) has shown significant enhancement in sensory characteristics[59]. Likewise, salted sardines (Sardina pilchardus), treated with lemon essential oil microemulsion received the highest scores for flavor and overall acceptability[46]. Berizi et al.[60] reported that a 10 g/kg concentration of methanolic pomegranate peel extract (MPPE) had the highest sensory rating and chewiness of chilled gutted rainbow trout. MPPE is, therefore, recommended as a natural agent to improve the textural properties of frozen fish during the first six months of storage. Panza et al.[61] adopted a zero- waste approach by utilizing the whole pomegranate (juice, peel, and seed) in varied proportions to find the effect on spoilage microorganisms and sensory quality of fish burgers. The researchers corroborated that pomegranate treated fish burgers had delayed microbial proliferation and maintained the sensory attributes with prolonged shelf life, due to the antibacterial action of tannins and phenolic acids present in the formulation.

      As far as the impact on sensory acceptability, the effect of oregano EO at 12.5 g/L on texture, color, and sensory acceptability of balls prepared from Tambaqui (Colossoma macropomum) fish was evaluated. It was found that OEO improved the color and aroma as sensory attributes[62]. This could be due to the antimicrobial and antioxidative properties of EOs. The EOs inhibit the H2S-producing bacteria, and chemical reactions which are responsible for the development of off-odors. Besides, when treated with thyme and star anise essential oil (1 g/L) at room temperature for 30 min, grass carp fillets had a less fishy smell and firmer texture than the control[4]. Although the above concentrations (v/v) were acceptable by the panelists.

      To overcome this, combination of various plant derived EOs is suggested, that possess high phenolic content but effective at low concentrations, so that their synergistic effect may offer better antimicrobial and antioxidant activities, and consequently maintaining the balance between sensory properties of fish products and odor factor of EOs. Encapsulation technique is also reported to be effective in masking the strong odor and flavor of EOs, as it (i) maintains the inherent flavor characteristics of food, (ii) prevents the evaporation of volatile compounds, (iii) enhances solubility for effective release and better distribution[11, 63]. It is recommended that materials used for encapsulation should have low reactivity with EOs, to ensure limited impact on the sensory attributes of foods.

    • Natural preservatives are safer and more effective agents for retarding the deterioration process of fish products. Because of this, plant-derived bioactive compounds and secondary metabolites, also called phytochemicals/green chemicals, with antioxidant and antimicrobial characteristics are now preferred over their synthetic counterparts. The application of phytochemicals as food additives extends the shelf life by delaying lipid oxidation and inhibiting microbial growth, thereby ensuring better nutritional value, and improved textural properties of fish and fish products. The increased demand for high quality fish products and the concept of 'Green consumerism' gaining momentum are boosting the application of bioactive phytochemicals, obtained from available, cheap, and underutilized resources. Modern and green extraction methods, including ultrasound-assisted extraction, microwave-assisted extraction, supercritical fluid extraction, and pressurized liquid extraction may be employed to obtain enhanced yields and stability of the phytochemicals. Further, the suitability of the phytochemicals, and their synergistic effect in combination with other natural preservatives or non-thermal technologies (irradiation, high pressure, retort pouch processing) and innovative packaging technologies may be explored to increase the degree of quality, functionality, sensory acceptability as well as shelf life of the fish and fish products, and thus meet consumer expectations.

    • Thanks to the Director, ICAR-Indian Veterinary Research Institute (IVRI), Izatnagar, Bareilly, India and the Station In-charge, Eastern Regional Station, ICAR-IVRI, Kolkata, India for their encouragement in writing this manuscript.

      • The authors declare that they have no conflict of interest.

      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Nanjing Agricultural University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (2)  Table (2) References (76)
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    Biswas O, Kandasamy P, Nanda PK, Biswas S, Lorenzo JM, et al. 2023. Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products. Food Materials Research 3:5 doi: 10.48130/FMR-2023-0005
    Biswas O, Kandasamy P, Nanda PK, Biswas S, Lorenzo JM, et al. 2023. Phytochemicals as natural additives for quality preservation and improvement of muscle foods: a focus on fish and fish products. Food Materials Research 3:5 doi: 10.48130/FMR-2023-0005

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