ORIGINAL ARTICLE
Effects of fruit tissue pH value on the Penicillium expansum growth, patulin accumulation and distribution
Min Wang,
Yamin Du,
Wenxiao Jiao,
Maorun Fu,
Min Wang
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorYamin Du
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorWenxiao Jiao
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorCorresponding Author
Maorun Fu
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Correspondence
Maorun Fu, College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250353, People's Republic of China.
Email: [email protected]
Search for more papers by this authorMin Wang,
Yamin Du,
Wenxiao Jiao,
Maorun Fu,
Min Wang
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorYamin Du
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorWenxiao Jiao
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Search for more papers by this authorCorresponding Author
Maorun Fu
College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, People's Republic of China
Correspondence
Maorun Fu, College of Food Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250353, People's Republic of China.
Email: [email protected]
Search for more papers by this authorMin Wang and Yamin Du contributed equally to this work.
Abstract
pH is an important environmental factor for the virulence of fungi. To explore the effect of tissue pH on the diffusion behavior of Penicillium expansum and patulin, pear (pH 4.98), apple (pH 3.72) and kiwifruit (pH 3.31) were selected to inoculate P. expansum. When the diameter of the lesion was 1 cm or 2 cm, tissues within a certain distance (0, 1, 2, and 3 cm) from the lesion were sampled. Results showed that low pH could inhibit the growth of P. expansum and hinder patulin accumulation in the decayed parts. The quantity of P. expansum was 1.99 × 105 CFU/g and patulin content was 13.84 mg/kg in pear, which were 6.86 times and 92.89 times of that in kiwi-fruit (lesion diameter 2 cm). In addition, the P. expansum colonies and patulin content decreased with the distance from the lesion, but there was no correlation between tissue pH and patulin distribution.
Novelty impact statement
- Low fruit tissue pH (pH < 4.98 ± 0.08) would inhibit the growth of Penicillium expansum and hinder the accumulation of patulin in the decayed parts.
- The pH value of the fruit tissue affects the diffusion behavior of P. expansum and patulin in different decayed fruits.
CONFLICTS OF INTEREST
The authors have declared no conflicts of interest for this article.
Open Research
DATA AVAILABILITY STATEMENT
The data presented in this study are available on request from the corresponding author.
REFERENCES
- Alkan, N., Espeso, E. A., & Prusky, D. (2013). Virulence regulation of phytopathogenic fungi by pH. Antioxidants & Redox Signaling, 19(9), 1012–1025. https://doi.org/10.1089/ars.2012.5062
- Arst, H. N., & Peñalva, M. A. (2003). pH regulation in Aspergillus and parallels with higher eukaryotic regulatory systems. Trends in Genetics, 19(4), 224–231. https://doi.org/10.1016/s0168-9525(03)00052-0
- Bandoh, S., Takeuchi, M., Ohsawa, K., Higashihara, K., Kawamoto, Y., & Goto, T. (2009). Patulin distribution in decayed apple and its reduction. International Biodeterioration & Biodegradation, 63(4), 379–382. https://doi.org/10.1016/j.ibiod.2008.10.010
- Barad, S., Sela, N., Kumar, D., Kumar-Dubey, A., Glam-Matana, N., Sherman, A., & Prusky, D. (2016). Fungal and host transcriptome analysis of pH-regulated genes during colonization of apple fruits by Penicillium expansum. BMC Genomics, 17, 330. https://doi.org/10.1186/s12864-016-2665-7
- Caracuel, Z., Roncero, M. I. G., Espeso, E. A., Gonzalez-Verdejo, C. I., Garcia-Maceira, F. I., & Di Pietro, A. (2003). The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Molecular Microbiology, 48(3), 765–779. https://doi.org/10.1046/j.1365-2958.2003.03465.x
- Cervantes-Chavez, J. A., Ortiz-Castellanos, L., Tejeda-Sartorius, M., Gold, S., & Ruiz-Herrera, J. (2010). Functional analysis of the pH responsive pathway Pal/Rim in the phytopathogenic basidiomycete Ustilago maydis. Fungal Genetics and Biology, 47(5), 446–457. https://doi.org/10.1016/j.fgb.2010.02.004
- Damoglou, A. P., & Campbell, D. S. (1986). The effect of pH on the production of patulin in apple juice. Letters in Applied Microbiology, 2(1), 9–11. https://doi.org/10.1111/j.1472-765X.1986.tb01504.x
- Drori, N., Kramer-Haimovich, H., Rollins, J., Dinoor, A., Okon, Y., Pines, O., & Prusky, D. (2003). External pH and nitrogen source affect secretion of pectate lyase by Colletotrichum gloeosporioides. Applied and Environmental Microbiology, 69(6), 3258–3262. https://doi.org/10.1128/AEM.69.6.3258-3262.2003
- Du, H., & Huang, G. (2016). Environmental pH adaption and morphological transitions in Candida albicans. Current Genetics, 62(2), 283–286. https://doi.org/10.1007/s00294-015-0540-8
- Enikova, R. K., Stoynovska, M. R., & Karcheva, M. D. (2020). Mycotoxins in fruits and vegetables. Journal of IMAB - Annual Proceeding (Scientific Papers), 26(2), 3139–3143. https://doi.org/10.5272/jimab.2020262.3139
10.5272/jimab.2020262.3139 Google Scholar
- Eshel, D., Miyara, I., Ailing, T., Dinoor, A., & Prusky, D. (2002). pH regulates endoglucanase expression and virulence of Alternaria alternata persimmon fruit. Molecular Plant-Microbe Interactions, 15(8), 774–779. https://doi.org/10.1094/mpmi.2002.15.8.774
- Ferreira-Nozawa, M. S., Silveira, H. C., Ono, C. J., Fachin, A. L., Rossi, A., & Martinez-Rossi, N. M. (2006). The pH signaling transcription factor PacC mediates the growth of Trichophyton rubrum on human nail in vitro. Medical Mycology, 44(7), 641–645. https://doi.org/10.1080/13693780600876553
- Li, B. Q., Lai, T. F., Qin, G. Z., & Tian, S. P. (2010). Ambient pH stress inhibits spore germination of Penicillium expansum by impairing protein synthesis and folding: A proteomic-based study. Journal of Proteome Research, 9(1), 298–307. https://doi.org/10.1021/pr900622j
- Li, B. Q., Qin, G. Z., & Tian, S. P. (2014). Mechanisms of ambient pH regulating spore germinability and pathogenicity of postharvest fungal pathogens (Vol. 7). Springer International Publishing Ag.
10.1007/978-3-319-07701-7_3 Google Scholar
- Li, B. Q., Wang, W. H., Zong, Y. Y., Qin, G. Z., & Tian, S. P. (2012). Exploring pathogenic mechanisms of Botrytis cinerea secretome under different ambient pH based on comparative proteomic analysis. Journal of Proteome Research, 11(8), 4249–4260. https://doi.org/10.1021/pr300365f
- Li, M. C., Martin, S. J., Bruno, V. M., Mitchell, A. P., & Davis, D. A. (2004). Candida albicans Rim13p, a protease required for Rim101p processing at acidic and alkaline pHs. Eukaryotic Cell, 3(3), 741–751. https://doi.org/10.1128/ec.3.3.741-751.2004
- Marin, S., Morales, H., Hasan, H. A., Ramos, A. J., & Sanchis, V. (2006). Patulin distribution in Fuji and Golden apples contaminated with Penicillium expansum. Food Additives & Contaminants, 23(12), 1316–1322. https://doi.org/10.1080/02652030600887610
- Martinez-Rossi, N. M., Persinoti, G. F., Peres, N. T., & Rossi, A. (2012). Role of pH in the pathogenesis of dermatophytoses. Mycoses, 55(5), 381–387. https://doi.org/10.1111/j.1439-0507.2011.02162.x
- Miyara, I., Shnaiderman, C., Meng, X., Vargas, W. A., Diaz-Minguez, J. M., Sherman, A., Thon, M., & Prusky, D. (2012). Role of nitrogen-metabolism genes expressed during pathogenicity of the alkalinizing colletotrichum gloeosporioides and their differential expression in acidifying pathogens. Molecular Plant-Microbe Interactions, 25(9), 1251–1263. https://doi.org/10.1094/mpmi-01-12-0017-r
- Morales, H., Barros, G., Marín, S., Chulze, S., Ramos, A. J., & Sanchis, V. (2008). Effects of apple and pear varieties and pH on patulin accumulation by Penicillium expansum. Journal of the Science of Food and Agriculture, 88(15), 2738–2743. https://doi.org/10.1002/jsfa.3401
- Nguyen Van Long, N., Vasseur, V., Coroller, L., Dantigny, P., Le Panse, S., Weill, A., Mounier, J., & Rigalma, K. (2017). Temperature, water activity and pH during conidia production affect the physiological state and germination time of Penicillium species. International Journal of Food Microbiology, 241, 151–160. https://doi.org/10.1016/j.ijfoodmicro.2016.10.022
- O'Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmüller, J., Alvarado-Balderrama, L., Bauser, C. A., Becker, C., Birren, B. W., Chen, Z., Choi, J., Crouch, J. A., Duvick, J. P., … Vaillancourt, L. J. (2012). Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics, 44(9), 1060–1065. https://doi.org/10.1038/ng.2372
- Ostry, V., Malir, F., Cumova, M., Kyrova, V., Toman, J., Grosse, Y., Pospichalova, M., & Ruprich, J. (2018). Investigation of patulin and citrinin in grape must and wine from grapes naturally contaminated by strains of Penicillium expansum. Food and Chemical Toxicology, 118, 805–811. https://doi.org/10.1016/j.fct.2018.06.022
- Prusky, D., Mcevoy, J. L., Saftner, R., Conway, W. S., & Jones, R. (2004). Relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit. Phytopathology, 94(1), 44–51.
- Puel, O., Galtier, P., & Oswald, I. P. (2010). Biosynthesis and toxicological effects of patulin. Toxins (Basel), 2(4), 613–631. https://doi.org/10.3390/toxins2040613
- Rossi, A., Cruz, A. H., Santos, R. S., Silva, P. M., Silva, E. M., Mendes, N. S., & Martinez-Rossi, N. M. (2013). Ambient pH sensing in filamentous fungi: pitfalls in elucidating regulatory hierarchical signaling networks. IUBMB Life, 65(11), 930–935. https://doi.org/10.1002/iub.1217
- Rychlik, M., & Schieberle, P. (2001). Model studies on the diffusion behavior of the mycotoxin patulin in apples, tomatoes, and wheat bread. European Food Research and Technology, 212(3), 274–278. https://doi.org/10.1007/s002170000255
- Saleh, I., & Goktepe, I. (2019). The characteristics, occurrence, and toxicological effects of patulin. Food and Chemical Toxicology, 129, 301–311. https://doi.org/10.1016/j.fct.2019.04.036
- Sun, C., Lin, M., Fu, D., Yang, J., Huang, Y., Zheng, X. D., & Yu, T. (2018). Yeast cell wall induces disease resistance against Penicillium expansum in pear fruit and the possible mechanisms involved. Food Chemistry, 241, 301–307. https://doi.org/10.1016/j.foodchem.2017.08.092
- Tannous, J., Atoui, A., El Khoury, A., Francis, Z., Oswald, I. P., Puel, O., & Lteif, R. (2016). A study on the physicochemical parameters for Penicillium expansum growth and patulin production: effect of temperature, pH, and water activity. Food Science & Nutrition, 4(4), 611–622. https://doi.org/10.1002/fsn3.324
- Tilburn, J., Sarkar, S., Widdick, D. A., Espeso, E. A., Orejas, M., Mungroo, J., & Arst, H. N. (1995). The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. The EMBO Journal, 14(4), 779–790. https://doi.org/10.1002/j.1460-2075.1995.tb07056.x
- Vylkova, S. (2017). Environmental pH modulation by pathogenic fungi as a strategy to conquer the host. PLoS Pathogens, 13(2), e1006149. https://doi.org/10.1371/journal.ppat.1006149
- Wang, F. L., Qiu, J. Y., Dai, M. X., Chen, L. L., Zhao, S. Z., Xin, X., & Zhou, Q. X. (2020). Isolation, identification and pathogenicity study of pathogens during post-harvest storage of sweet cherries. Journal of Zhejiang University (Agriculture and Life Sciences), 46(1), 126–134. https://doi.org/10.3785/j.issn.1008-9209.2019.10.111
- Wang, Y., Shan, T. T., Yuan, Y. H., Zhang, Z. W., Guo, C. F., & Yue, T. L. (2017). Evaluation of Penicillium expansum for growth, patulin accumulation, nonvolatile compounds and volatile profile in kiwi juices of different cultivars. Food Chemistry, 228, 211–218. https://doi.org/10.1016/j.foodchem.2017.01.086
- Wei, C. Z., Yu, L. L., Qiao, N. Z., Zhao, J. X., Zhang, H., Zhai, Q. X., Tian, F. W., & Chen, W. (2020). Progress in the distribution, toxicity, control, and detoxification of patulin: A review. Toxicon, 184, 83–93. https://doi.org/10.1016/j.toxicon.2020.05.006
- Wei, D. M., Xu, J., Dong, F. S., Liu, X. G., Wu, X. H., & Zheng, Y. Q. (2017). Penicillium and patulin distribution in pears contaminated with Penicillium expansum. Determination of patulin in pears by UHPLC-MS/MS. Journal of Integrative Agriculture, 16(7), 1645–1651. https://doi.org/10.1016/s2095-3119(16)61543-5
- Zheng, X. F., Wei, W. N., Zhou, W. Y., Li, H. X., Rao, S. Q., Gao, L., & Yang, Z. Q. (2021). Prevention and detoxification of patulin in apple and its products: A review. Food Research International, 140, 110034. https://doi.org/10.1016/j.foodres.2020.110034
- Zong, Y. Y., Li, B. Q., & Tian, S. P. (2015). Effects of carbon, nitrogen and ambient pH on patulin production and related gene expression in Penicillium expansum. International Journal of Food Microbiology, 206, 102–108. https://doi.org/10.1016/j.ijfoodmicro.2015.05.007
