Exploring the Citrus Sour Rot pathogen: biochemical aspects, virulence factors, and strategies for disease management - a review

Abe, 1948, Ergot fungus. IX. Separation of an active substance and its properties, J. Agric. Chem. Soc. Jpn., 22, 2 Azizan, 2016, Fungal metabolites and their industrial importance: A brief review, Malays. J. Biochem. Mol. Biol., 2, 15 Barth, 2009, Microbiological spoilage of fruits and vegetables, 135 Baudoin, 1982, Factors influencing the susceptibility of lemons infection by Geotrichum candidum, Phytopathology, 72, 1592, 10.1094/Phyto-72-1592 Bazioli, 2019, Biological control of citrus postharvest phytopathogens, Toxins, 11, 460, 10.3390/toxins11080460 Bockelmann, 2011, Cheese - Smear-ripened cheeses, 753 Boubaker, 2019, Study of essential oil composition and antifungal activity of Lavandula mairei, L. dentate and Tetraclinis articulata, J. Appl. Sci., 19, 544, 10.3923/jas.2019.544.550 Buchta, 1988, Geotrichum candidum - an opportunistic agent of mycotic diseases, Mycoses, 31, 363, 10.1111/j.1439-0507.1988.tb04432.x Butler, 1988, Galactomyces citri-aurantii a newly found teleomorph of Geotrichum citri-aurantii. The cause of sour rot of citrus fruit, Mycotaxon, 33, 197 Butler, 1972, Endomyces geotrichum a perfect state of Geotrichum candidum, Mycologia, 64, 365, 10.1080/00275514.1972.12019270 Calvo, 2002, Relationship between secondary metabolism and fungal development, Microbiol. Mol. Biol. Rev., 66, 447, 10.1128/MMBR.66.3.447-459.2002 Chaudhari, 2016, Phenyllactic acid: a potential antimicrobial compound in lactic acid bacteria, J. Bacteriol. Mycol., 2, 121 Chen, 2019, Inhibition of key citrus postharvest fungal strains by plant extracts in vitro and in vivo: A review, Plants, 8, 26, 10.3390/plants8020026 Cissé, 2013, Genome sequencing of the plant pathogen Taphrina deformans, the causal agent of peach leaf curl, mBio, 4, 10.1128/mBio.00055-13 Costa, 2019, Penicillium digitatum infection mechanisms in citrus: What do we know so far?, Fungal Biol, 123, 584, 10.1016/j.funbio.2019.05.004 Del Rio, 1998, Citrus polymethoxylated flavones can confer resistance against Phytophthora citrophthora, Penicillium digitatum, and Geotrichum species, J. Agric. Food Chem., 46, 4423, 10.1021/jf980229m Dieuleveux, 1998, Purification and characterization of anti-Listeria compounds produced by Geotrichum candidum, Appl. Environ. Microbiol., 64, 800, 10.1128/AEM.64.2.800-803.1998 Droby, 1992, Biological control of postharvest diseases: A promising alternative to the use of synthetic fungicides, Phytoparasitica, 20, 149S, 10.1007/BF02980427 Droby, 1998, Commercial testing of Aspire: a yeast preparation for the biological control of postharvest decay of citrus, Biol. Control, 12, 97, 10.1006/bcon.1998.0615 Durbin, 1991, Bacterial phytotoxins: Mechanisms of action, Experentia, 47, 776, 10.1007/BF01922457 Eckert, 1985, The chemical control of postharvest diseases: Subtropical and tropical fruits, Annu. Rev. Phytopathol., 23, 421, 10.1146/annurev.py.23.090185.002225 Eckert, 1978, Postharvest disorders and diseases of citrus fruit, Outlook Agric., 9, 225, 10.1177/003072707800900506 Egarnes, 2017, Treatment with the NR4A1 agonist cytosporone B controls influenza virus infection and improves pulmonary function in infected mice, PLoS One, 12, 10.1371/journal.pone.0186639 Eliskases-Lechner, 2011, Yeasts and Molds - Geotrichum candidum, 765 El-Otmani, 2011, Citrus spp.: Orange mandarin tangerin clementine grapefruit pomelo lemon and lime, 437 El Refai, 1970, The alkaloids of fungi. I. The formation of ergoline alkaloids by representative mold fungi, Jpn. J. Microbiol., 14, 91, 10.1111/j.1348-0421.1970.tb00496.x Fabiola, 2017, Inhibition of an extracellular polygalacturonase from Ceotrichum candidum by a proteinaceous inhibitor isolated from lemon fruits, J. Microbiol. Biotechnol. Food Sci., 6, 1019, 10.15414/jmbfs.2017.6.4.1019-1025 Fallik, 2021, Hot water rinsing and brushing of fresh produce as an alternative to chemical treatment after harvest—The story behind the technology, Agronomy, 11, 1653, 10.3390/agronomy11081653 Fei, 2016, Metabolic and transcriptomic profiling of Streptococcus intermedius during aerobic and anaerobic growth, Metabolomics, 12, 46, 10.1007/s11306-016-0966-0 Ferraz, 2016, Biocontrol ability and putative mode of action of yeasts against Geotrichum citri-aurantii in citrus fruit, Microbiol. Res., 188–189, 72, 10.1016/j.micres.2016.04.012 Figueredo, 2011, Geotrichum candidum as etiological agent of horse dermatomycosis, Vet. Microbiol., 148, 368, 10.1016/j.vetmic.2010.09.025 Food and Agriculture Organization of the United Nations, 2019 Gente, 2006, Identification of Geotrichum candidum at the species and strain level: proposal for a standardized protocol, J. Ind. Microbiol. Biotechnol., 33, 1019, 10.1007/s10295-006-0130-3 Gopinath, 2005, Extracellular enzymatic activity profiles in fungi isolated from oil-rich environments, Mycoscience, 46, 119, 10.1007/S10267-004-0221-9 Hao, 2010, Control of citrus postharvest green and blue mold and sour rot by tea saponin combined with imazalil and prochloraz, Postharvest Biol. Technol., 56, 39, 10.1016/j.postharvbio.2009.10.003 Harvey, 1972, 26 Hiwatashi, 2018, The effects of cytosporone-B, a novel antifibrotic agent, on vocal fold fibroblasts, Laryngoscope, 128, E425, 10.1002/lary.27361 Hollomon, 2015, Fungicide resistance: 40 years on and still a major problem, 3 Hoog, 1998, Galactomyces Redhead & Malloch, 209 Horita, 2016, Sour rot of carrot caused by Geotrichum candidum in Japan, J. Gen. Plant Pathol., 82, 65, 10.1007/s10327-015-0638-3 Hulvová, 2013, Parasitic fungus Claviceps as a source for biotechnological production of ergot alkaloids, Biotechnol. Adv., 31, 79, 10.1016/j.biotechadv.2012.01.005 Isshiki, 2001, Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata, Mol. Plant Microbe Interact., 14, 749, 10.1094/MPMI.2001.14.6.749 Jakovljević, 2018, Potential of pure and mixed cultures of Cladosporium cladosporioides and Geotrichum candidum for application in bioremediation and detergent industry, Saudi J. Biol. Sci., 25, 529, 10.1016/j.sjbs.2016.01.020 Janisiewicz, 2002, Biological control of postharvest diseases of fruits, Annu. Rev. Phytopathol., 40, 411, 10.1146/annurev.phyto.40.120401.130158 Karim, 2016, Antifungal properties of organic extracts of eight Cistus L. species against postharvest citrus sour rot, Lett. Appl. Microbiol., 62, 16, 10.1111/lam.12507 Kawtharani, 2020, Phenyllactic acid produced by Geotrichum candidum reduces Fusarium sporotrichioides and F. langsethiae growth and T-2 Toxin concentration, Toxins, 12, 209, 10.3390/toxins12040209 Kim, 1999, Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes, Appl. Environ. Microbiol., 65, 1029, 10.1128/AEM.65.3.1029-1035.1999 Kim, 2011, First report of sour rot on post-harvest oriental melon, tomato, cucumber, potato, pumpkin and carrot caused by Geotrichum candidum, Res. Plant Dis., 17, 232, 10.5423/RPD.2011.17.2.232 Klein, 2018, Biofilm production by Aureobasidium pullulans improves biocontrol against sour rot in citrus, Food Microbiol., 69, 1, 10.1016/j.fm.2017.07.008 Klewicka, 2016, Ellagitannins from raspberry (Rubus idaeus L.) fruit as natural inhibitors of Geotrichum candidum, Molecules, 21, 908, 10.3390/molecules21070908 Lahlali, 2004, Efficacy assessment of Candida oleophila (strain O) and Pichia anomala (strain K) against major postharvest diseases of citrus fruits in Morocco, Comm. Appl. Biol. Sci., 69, 601 Lassois, 2008, Biological control of crown rot of bananas with Pichia anomala strain K and Candida oleophila strain O, Biol. Control, 45, 410, 10.1016/j.biocontrol.2008.01.013 Leahy, 2014, Biopesticide oversight and registration at the U.S. Environmental Protection Agency, 3 Leneveu-Jenvrin, 2020, Role of biological control agents and physical treatments in maintaining the quality of fresh and minimally-processed fruit and vegetables, Crit. Rev. Food Sci. Nutr., 60, 2837, 10.1080/10408398.2019.1664979 Leyva-Jimenez, 2019, Potential antimicrobial activity of honey phenolic compounds against Gram positive and Gram negative bacteria, LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.), 101, 236, 10.1016/j.lwt.2018.11.015 Lima, 1997, Effectiveness of Aureobasidium pullulans and Candida oleophila against postharvest strawberry rots, Postharvest Biol. Technol., 10, 169, 10.1016/S0925-5214(96)01302-6 Liu, 2017, Polygalacturonase gene pgxB in Aspergillus niger is a virulence factor in apple fruit, PLoS One, 12 Liu, 2010, Biological control of postharvest sour rot of citrus by two antagonistic yeasts, Lett. Appl. Microbiol., 51, 30 Liu, 2009, Antifungal activity of thyme oil against Geotrichum citri-aurantii in vitro and in vivo, J. Appl. Microbiol., 107, 1450, 10.1111/j.1365-2672.2009.04328.x Liu, 2019, Different mechanisms of action of isolated epiphytic yeasts against Penicillium digitatum and Penicillium italicum on citrus fruit, Postharvest Biol. Technol., 152, 100, 10.1016/j.postharvbio.2019.03.002 Lubna, 2018, Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid, J. Plant Interact., 13, 100, 10.1080/17429145.2018.1436199 Maione, 2017, Finding the most significant elements for the classification of organic orange leaves: A data mining approach, Anal. Lett., 50, 2292, 10.1080/00032719.2017.1286667 Maldonado, 2016, A review on Geotrichum lipases: Production, purification, immobilization and applications, Chem. Biochem. Eng. Q., 30, 439, 10.15255/CABEQ.2016.907 Martínez-Blay, 2020, Control of major citrus postharvest diseases by sulfur-containing food additives, Int. J. Food Microbiol., 330, 108713, 10.1016/j.ijfoodmicro.2020.108713 McEvoy, 1974, Phenylalanine hydroxylase activity in a mutant of Geotrichum candidum, Antonie Leeuwenhoek, 40, 409, 10.1007/BF00399353 McKay, 2012, Distinguishing Galactomyces citri-aurantii from G. geotrichum and characterizing population structure of the two postharvest sour rot pathogens of fruit crops in California, Phytopathology, 102, 528, 10.1094/PHYTO-05-11-0156 Mercier, 2005, Control of green mold and sour rot of stored lemon by biofumigation with Muscodor albus, Biol. Control, 32, 401, 10.1016/j.biocontrol.2004.12.002 Montesinos-Herrero, 2010, Combination of physical and low-toxicity chemical postharvest treatments for integrated disease management of citrus fruit: a review, Stewart Postharvest Rev, 1, 1 Muhammad, 2019, Purification, characterization and thermodynamic assessment of an alkaline protease by Geotrichum candidum of dairy origin, Iran. J. Biotechnol., 17, 10.21859/ijb.2042 Mullen, 2003, Analysis of ellagitannins and conjugates of ellagic acid and quercetin in raspberry fruits by LC–MSn, Phytochemistry, 64, 617, 10.1016/S0031-9422(03)00281-4 Mu, 2012, Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound, Appl. Microbiol. Biotechnol., 95, 1155, 10.1007/s00253-012-4269-8 Nakajima, 2014, Virulence factors of Botrytis cinerea, J. Gen. Plant Pathol., 80, 15, 10.1007/s10327-013-0492-0 Nakamura, 2003, Polygalacturonase S31PG1 from Geotrichum candidum citrus race S31 expressed in Schizosaccharomyces pombe versus S31PG2 regarding soft rot on lemon fruit, J. Gen. Plant Pathol., 69, 283, 10.1007/s10327-003-0048-9 Nakamura, 2019, Functions and mechanisms: polygalacturonases from plant pathogenic fungi as pathogenicity and virulence factors, J. Gen. Plant Pathol., 85, 243, 10.1007/s10327-019-00856-8 Nakamura, 2001, Comparison of endo-polygalacturonase activities of citrus and non-citrus races of Geotrichum candidum, and cloning and expression of the corresponding genes, Mol. Plant Pathol., 2, 265, 10.1046/j.1464-6722.2001.00075.x Naz, 2013, Aromatic amino acids as precursors of antimicrobial metabolites in Geotrichum candidum, FEMS Microbiol. Lett., 344, 39, 10.1111/1574-6968.12152 Nazerian, 2013, Association of Geotrichum citri-aurantii with citrus fruits decay in Iran, Int. J. Agron. Plant Prod., 4, 1839 2020 Nielsen, 1998, Colony interaction and secondary metabolite production of cheese-related fungi in dual culture, J. Food Protect., 61, 1023, 10.4315/0362-028X-61.8.1023 Ng, 2019, Antimicrobial and antioxidant activities of phenolic metabolites from flavonoid-producing yeast: Potential as natural food preservatives, Food Chem., 270, 123, 10.1016/j.foodchem.2018.07.077 Nunes, 2012, Biological control of postharvest diseases of fruit, Eur. J. Plant Pathol., 133, 181, 10.1007/s10658-011-9919-7 Oeser, 2002, Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction, Fungal Genet. Biol., 36, 176, 10.1016/S1087-1845(02)00020-8 Ohhira, 2004, Identification of 3-phenyllactic acid as a possible antibacterial substance produced by Enterococcus faecalis TH10, Biocontrol Sci. Technol., 9, 77, 10.4265/bio.9.77 Ortuño, 2011, Comparative study of flavonoid and scoparone accumulation in different Citrus species and their susceptibility to Penicillium digitatum, Food Chem., 125, 232, 10.1016/j.foodchem.2010.09.012 OuYang, 2019, Cinnamaldehyde exerts its antifungal activity by disrupting the cell wall integrity of Geotrichum citri-aurantii, Front. Microbiol., 10, 55, 10.3389/fmicb.2019.00055 Pazouki, 2000, Understanding the morphology of fungi, Bioprocess Eng., 22, 127, 10.1007/s004490050022 Pérez-Alfonso, 2012, The effects of essential oils carvacrol and thymol on growth of Penicillium digitatum and P. italicum involved in lemon decay, Int. J. Food Microbiol., 158, 101, 10.1016/j.ijfoodmicro.2012.07.002 Pontes, 2020, Virulence factors in the phytopathogen−host interactions: An overview, J. Agric. Food Chem., 68, 7555, 10.1021/acs.jafc.0c02389 Pottier, 2008, Safety assessment of dairy microorganisms: Geotrichum candidum, Int. J. Food Microbiol., 126, 327, 10.1016/j.ijfoodmicro.2007.08.021 Prusky, 2004, Relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit, Phytopathology, 94, 44, 10.1094/PHYTO.2004.94.1.44 Qi, 2018, Determination of metabolites of Geotrichum citri-aurantii treated with peppermint oil using liquid chromatography mass spectrometry and gas chromatography-mass-spectrometry, J. Food Biochem., 43 Ramezanian, 2016, Effect of Zataria multiflora Boiss and Thymus vulgaris L. essential oils on black rot of ‘Washington Navel’ orange fruit, Postharvest Biol. Technol., 112, 152, 10.1016/j.postharvbio.2015.10.011 Reineke, 2008, Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation, Mol. Plant Pathol., 9, 339, 10.1111/j.1364-3703.2008.00470.x Saito, 2017, Prevalence of postharvest diseases of mandarin fruit in California, Plant Health Prog., 18, 204, 10.1094/PHP-08-17-0048-RS Sallam, 1970, The alkaloids of fungi - 2. Some factors influencing alkaloid formation by Geotrichum candidum, J. Basic Microbiol., 10, 405 Samorini, 1997, Aspergillus fumigatus Fres.g, Eleusis, 8, 38 Serna-Escolano, 2020, Thymol encapsulated into HP-β-Cyclodextrin as an alternative to synthetic fungicides to induce lemon resistance against sour rot decay, Molecules, 25, 4348, 10.3390/molecules25184348 Shahab, 2009, Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs, Afr. J. Agric. Res., 4, 1312 Shapiro-Ilan, 2005, Definitions of pathogenicity and virulence in invertebrate pathology, J. Invertebr. Pathol., 88, 1, 10.1016/j.jip.2004.10.003 Smilanick, 2008, Control of citrus postharvest green mold and sour rot by potassium sorbate combined with heat and fungicides, Postharvest Biol. Technol., 47, 226, 10.1016/j.postharvbio.2007.06.020 Smilanick, 2007, Influence of temperature and humidity on survival of Penicillium digitatum and Geotrichum citri-aurantii, Plant Dis., 91, 990, 10.1094/PDIS-91-8-0990 Smith, 1917, Sour rot of lemon in California, Phytopathology, 7, 37 Sparks, 2018, Crop protection discovery: Is being the first best?, J. Agric. Food Chem., 66, 10337, 10.1021/acs.jafc.8b03484 Stevens, 1996, Plant hormesis induced by ultraviolet light-C for controlling postharvest diseases of tree fruits, Crop Protect., 15, 129, 10.1016/0261-2194(95)00082-8 Sui, 2020, Genome sequence, assembly, and characterization of the antagonistic yeast Candida oleophila used as a biocontrol agent against post-harvest diseases, Front. Microbiol., 11, 295, 10.3389/fmicb.2020.00295 Tang, 2018, Antifungal mechanism of sodium dehydroacetate against Geotrichum citri-aurantii, World J. Microbiol. Biotechnol., 34, 29, 10.1007/s11274-018-2413-z Teló, 2017, Fungicide and insecticide residues in rice grains, Acta Sci. Agron., 39, 9, 10.4025/actasciagron.v39i1.30594 Thomas, 2004, Pathogenicity and virulence, J. Invertebr. Pathol., 85, 146, 10.1016/j.jip.2004.01.006 Thornton, 2010, Detection of the sour-rot pathogen Geotrichum candidum in tomato fruit and juice by using a highly specific monoclonal antibody-based ELISA, Int. J. Food Microbiol., 143, 166, 10.1016/j.ijfoodmicro.2010.08.012 Tiunova, 1982, ß-Glucanases of Geotrichum candidum, Mikrobiologiya, 51, 427 Tsujisaka, 1973, Induced formation of lipase by Geotrichum candidum Link, Agric. Biol. Chem., 37, 837 Usall, 2016, Physical treatments to control postharvest diseases of fresh fruits and vegetables, Postharvest Biol. Technol., 122, 30, 10.1016/j.postharvbio.2016.05.002 Valerio, 2004, Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation, FEMS Microbiol. Lett., 233, 289, 10.1111/j.1574-6968.2004.tb09494.x Vikari, 2009, Forest products: Biotechnology in pulp and paper processing, 80 Vilanova, 2018, Differential contribution of the two major polygalacturonases from Penicillium digitatum to virulence towards citrus fruit, Int. J. Food Microbiol., 282, 16, 10.1016/j.ijfoodmicro.2018.05.031 Wang, 2020, Biocontrol ability and action mechanism of Metschnikowia citriensis against Geotrichum citri-aurantii causing sour rot of postharvest citrus fruit, Food Microbiol., 87, 103375, 10.1016/j.fm.2019.103375 Wang, 2018, Control of citrus post-harvest green molds, blue molds, and sour rot by the cecropin A-melittin hybrid peptide BP21, Front. Microbiol., 9, 2455, 10.3389/fmicb.2018.02455 Waqas, 2012, Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress, Molecules, 17, 10754, 10.3390/molecules170910754 Xu, 1983, Comparative study of pH and nitrogen sources on the extracellular protein and polypeptide production by Rhodotorula rubra and Geotrichum candidum strains, Acta Mycol. Sin., 2, 127 Xu, 2012, In vitro and In vivo antifungal activity of a water-dilutable cassia oil microemulsion against Geotrichum citri-aurantii, J. Sci. Food Agric., 92, 2668, 10.1002/jsfa.5686 Yaghmour, 2012, Biology and sources of inoculum of Geotrichum candidum causing sour rot of peach and nectarine fruit in California, Plant Dis., 96, 204, 10.1094/PDIS-05-11-0391 Yamada, 1990, Detection of indoleacetic acid biosynthesis in some species of Taphrina causing hyperplastic diseases in plants, Ann. Phytopathol. Soc. Jpn., 56, 532, 10.3186/jjphytopath.56.532 Yasser, 2019, Effect of hot water treatment on postharvest fruit rots and quality of tomato fruits, Plant Arch, 19, 2325 Yin, 2019, Cytosporone B as a biological preservative purification fungicidal activity and mechanism of action against Geotrichum citri-aurantii, Biomolecules, 9, 125, 10.3390/biom9040125 Ząbek, 2017, Biodiversity in targeted metabolomics analysis of filamentous fungal pathogens by 1H NMR-based studies, World J. Microbiol. Biotechnol., 33, 132, 10.1007/s11274-017-2285-7 Zhao, 2020, Genome sequencing and transcriptome analysis of Geotrichum citri-aurantii on citrus reveal the potential pathogenic- and guazatine-resistance related genes, Genomics, 112, 4063, 10.1016/j.ygeno.2020.07.013 Zhong, 2020, Citrus origin diffusion and economic importance, 5, 10.1007/978-3-030-15308-3_2 Zutz, 2016, Valproic acid induces antimicrobial compound production in Doratomyces microsporus, Front. Microbiol., 7, 510, 10.3389/fmicb.2016.00510