In plants melanin acts as a reinforcer of cell walls and cuticle, increasing the resistance of plants to microbial and viral infection (Guo et al., 2023; Riley 1997). Melanin may kill microbes through the production of toxic intermediates and oxidative damage (Smith et al., 2022). The form of pigment found in plant is phytomelanin or phytomelan (De-Paula et al., 2013). Phytomelanin is present in seed coat of Asparagales, Asteraceae species and in fruits of few Compositae (De-Paula et al., 2013; Ozdemir and Keles 2018). Melanin is derived from the Greek word “melanos” meaning black though some melanin may be very dark, brown or even yellow (Pralea et al., 2019; Guo et al., 2023). Broadly melanin is classified into five types- eumelanin, pheomelanin, neuromelanin, allomelanin and pyomelanin- based on various chemical precursors used in biosynthesis (Cao et al., 2021). Eumelanin is dark brown/black, pheomelanin yellow/red and allomelanin, specific to plant kingdom (Pralea et al., 2019). Nitrogen-deficient plant and fungal melanin is often called allomelanin (black pigment) (Ozdemir and Keles 2018; Guo et al., 2023). Melanin is present in fungi, bacteria, insect, animals, plants, marine animals and mammals (Castro-Sowinski et al., 2002; Lerner and Fitzpatrick 1950). The function of melanin includes pigmentation, radical scavenging, radiation protection and thermal regulation (Cao et al., 2021).
Phytomelanin has no physical structure of its own but assumes its morphology as it fills intercellular spaces in the pericarp between hypodermis and sclerenchyma (Pandey and Dhakal 2001). Phytomelanin layer contribute to pericarp strength which provides mechanical resistance to biotic and abiotic stress (Jockovic et al., 2020). Nick (2021) shows that phytomelanin is made in plastids in parenchymatic cells that differentiates into sclereids, lignified support cells that undergoes programmed cell death to fulfill their function. Melanin pigment is found in many fungal species. It can absorb a wide spectrum of electromagnetic radiation and transduce this radiation into other form of energy. The ability of melanotic fungi to harvest energy would make them autotrophs and place them alongside plants that contribute to the conversion of solar and physical electromagnetic energy sources into biologically useful energy (Casadevall et al., 2017).
Melanin production contributes to microbial pathogenesis owing to its potential for protection against host defense systems (Nosanchuk and Casadevall 2003; Alp 2010). Destruction or inhibition of synthesis of the melanin by biocontrol agent (BCA) can be a biological control measure (Butler et al., 2005). Plant pathogen Verticillium dahlia produces heavily melanized microsclerotia that can survive for more than 14 years (Li et al., 2022). One of the alternative control measures is identification of gene that controls or inhibits reproduction and formation of survival structures (Li et al., 2022). Reducing the primary inoculum in the soil can be accomplished by many management strategies. Colonization of plant roots by beneficial microbes in the rhizosphere is a stimulus that may result in induced systemic resistance (ISR) which may have a positive effect on the ability of plant to defend itself from the pathogenic invasion (Hilker et al., 2016). The chemical communication in the rhizosphere results in ISR/rhizomicrobe plant priming of defense (Mhlongo et al., 2018). The signalomics describes metabolomics approaches may decipher chemical communication. The induced resistance is a working mechanism of the BCA. Plant and rhizosphere microbes secrete compounds that are beneficial to each other to establish interaction and relationship. The below ground interaction, primes plant against biotic and abiotic stresses. Perception of the priming stimulus leads to activation of signaling molecules, primary metabolism regulation and gene activation of enzyme involved in production of secondary defense metabolites (Mhlongo et al., 2018). The biocontrol bacterium Paenibacillus alvei K165 protects Arabidopsis thaliana from plant pathogen Verticillium dahliae. This P. alvei K165 mediated protection resulted from ISR in A. thaliana plant (Tjamos et al., 2005). The biocontrol agents Paenibacillus alvei K-165 and Fusarium oxysporum F2 induced pathogenesis-related (PR) proteins PR-1 and PR-4 in stem of eggplant protecting plant from Verticillium dahliae. Production of PR-1 and PR-4 revealed correlation with the rhizosphere population of biocontrol agents (Angelopoulou et al.,2014). The resistance induced by the strain P. alvei K165 is dependent on both salicylate and jasmonate-dependent defense pathway as evidenced by transient accumulation of PR-1 and plant defensin1.2 transcript in the aerial part of the infected plant (Gkizi et al., 2016). Applying bacterial or fungal BCA as a soil amendment reduced disease development and primed plant defense.
References:
Alp, S. 2010 Melanin and its Role on the Virulence of Cryptococcus neoformans. Mikrobiyol. Bul. 44(3): 519 – 526
PMID: 21064003
Angelopoulou, D. J., Naska, E. J., Paplomatas, E. J. and Tjamos, S. E. 2014 Biological Control Agents (BCAs) of Verticillium Wilt: Influence of Application Rates and Delivery Method on Plant Protection, Triggering of Host Defence Mechanisms and Rhizosphere Populations of BCAs. Plant Pathol. 63(5): 1062 – 1069
doi.org/10.1111/ppa.12198
Butler, M. J., Gardiner, R. B. and Day, A.W. 2005 Degradation of Melanin or Inhibition of its Synthesis: Are these a Significant Approach as a Biological Control of Phytopathogenic Fungi? Biological Control 32(2): 326 – 336
doi.org/10.1016/j.biocontrol.2004.08.008
Cao, W., Zhou, X., McCallum, N. C., Hu, Z., Ni, Q. Z., Kapoor, U., Heil, C. M., Cay, K. S., Zand, T., Mantanona, A. J., Jayaraman, A., Dhinojwala, A., Deheyn, D. D., Shawkey, M. D., Burkart, M. D., Rinehart, J. D. and Gianneschi, N. C. 2021 Unraveling the Structure and Function of Melanin through Synthesis. J. Am. Chem. Sci. 143(7): 2622 – 2637
doi.org/10.1021/jacs.0c12322
Casadevall, A., Cordero, R. J. B., Bryan, R., Nosanchuk, J. and Dadachova, E. 2017 Melanin Radiation and Energy Transduction in Fungi. Microbial Spectrum 5(2): FUNK-0037-2016
doi: 10.1128/microbiolspec.funk-0037-2016
Castro-Sowinski, S., Martinez-Drets, G. and Okon, Y. 2002 Laccase Activity in Melanin-Producing Strains of Sinorhizobium meliloti. FEMS Microbiol. Lett. 209(1): 119 – 125
doi.org/10.1111/j.1574-6968.2002.tb11119.x
De-Paula, O. C., Marzinek, J., Oliveira, D. M. T. and Machado, S. R. 2013 The Role of Fibres and Hypodermis in Compositae Melanin Secretion. Micron. 44: 312 – 316
doi: 10.1016/j.micron.2012.08.003
Gkizi, D., Lehmann, S., L’Haridon, F., Serrano, M., Paplomatas, E. J., Metraux, J-P. and Tjamos, S. E. 2016 The Innate Immune Signaling System as a Regulator of Disease Resistance and Induced Systemic Resistance Activity against Verticillium dahliae. MPMI 29(4): 313 – 323
doi.org/10.1094/MPMI-11-15-0261-R
Guo, L., Li, W., Gu, Z., Wang, L., Guo, L., Ma, S., Li, C., Sun, J., Han, B. and Chang, J. 2023 Recent Advances and Progress on Melanin: From Source to Application. Int. J. Mol. Sci. 24(5): 4360
doi: 10.3390/ijms24054360
Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Baurle, I., Geiselhardt, S., Hincha, D. K., Kunze, R., Mueller-Roeber, B., Rillig, M. C., Rolff, J., Romeis, T., Schmulling, T., Steppuhn, A., van Dongen, J., Whitcomb, S. J., Wurst, S., Zuther, E. and Koopka, J. 2016 Priming and Memory of Stress Responses in Organisms Lacking a Nervous System. Biol. Rev. 91(4): 1118 – 1133
doi.org/10.1111/brv.12215
Jockovic, J., Rajcevic, N., Terzic, S., Zoric, L., Jockovic, M., Miladinovic, D. and Lukovic, J. 2020 Pericarp Features of Wild Perennial Helianthus L. Species as a Potential Source for Improvement of Technical and Technological Properties of Cultivated Sunflower. Industrial Crops and Product 144: 112030
doi.org/10.1016/j.indcrop.2019.112030
Lerner, A. B. and Fitzpatrick, T. B. 1950 Biochemistry of Melanin Formation. Physiol. Rev. 30(1): 91 – 126
doi: 10.1152/physrev.1950.30.1.91
Li, H., Wang, D., Zhang, D-D., Geng, Q., Li, J-J., Sheng, R-C., Xue, H-S., Zhu, H., Kong, Z-Q., Dai, X-F., Klosterman, S. J., Subbarao, K. V., Chen, F-M. and Chen, J-Y. 2022 A Polyketide Synthase from Verticillium dahliae Modulates Melanin Biosynthesis and Hyphal Growth to Promote Virulence. BMC Biol. 20(1): 125
doi: 10.1186/s12915-022-01330-2
Mhlongo, M. I., Piater, L. A., Madala, N. E., Labuschagne, N. and Dubery, I. A. 2018 The Chemistry of Plant-Microbe Interactions in Rhizosphere and the Potential for Metabolomics to Reveal Signaling Related to Defense Priming and Induced Systemic Resistance. Front Plant Sci. 9: 112
doi: 10.3389/fpls.2018.00112
Nosanchuk, J. D. and Casadevall, A. 2003 The Contribution of Melanin to Microbial Pathogenesis. Cellular Microbiol. 5(4): 203 – 223
doi.org/10.1046/j.1462-5814.2003.00268.x
Nick, P. 2021 Black is Beautiful (and Protective): Melanin Synthesis in Animals and Plants. Protoplasma 258: 923 – 924
doi.org/10.1007/s00709-021-01693-3
Ozdemir, O. and Keles, Y. 2018 Extraction, Purification, Antioxidant Properties and Stability Condition of Pheomelanin Pigment on the Sunflower Seeds. IJSM 5(2): 140 – 148
doi: 10.21448/ijsm.377470
Pandey, A. and Dhakal, M. R. 2001 Phytomelanin in Compositae. Curr. Sci. 80(8): 933 – 940
http://www.jstor.org/stable/24105803
Pralea, I-E., Moldovan, R-C., Petrache, A-M., Llies, M., Heghes, S-C., Lelciu, I., Nicoara, R., Moldovan, M., Ene, M., Radu, M., Uifalean, A. and Luga, C-A. 2019 From Extraction to Advanced Analytical Methods: The Challenges of Melanin Analysis. Int. J. Mol. Sci. 20(16): 3943
doi: 10.3390/ijms20163943
Riley, P. A. 1997 Melanin. The International J. Biochem. Cell Biol. 29(11): 1235 – 1239
doi.org/10.1016/S1357-2725(97)00013-7
Smith, D. F. Q., Dragotakes, Q., Kulkarni, M., Hardwick, J. M. and Casadevall, A. 2022 Melanization is an Important Antifungal Defense Mechanism in Galleria mellonella Hosts. CC BY-NC 4.0 International License
doi: 10.1101/2022.04.02.486843
Tjamos, S. E., Flemetakis, E., Paplomatas, E. J. and Katinakis, P. 2005 Induction of Resistance to Verticillium dahliae in Arabidopsis thaliana by the Biocontrol Agent K-165 and Pathogenesis-Related Proteins Gene Expression. MPMI 18(6): 555 – 561
doi.org/10.1094/MPMI-18-0555