[en] AbstractMicrobial activity is a primary cause of postharvest deterioration in fresh-eating jujubes, but the mechanisms underlying microbiota-driven decay remain poorly defined. This study investigated the dynamics of endophytic and epiphytic microbial communities on jujube fruit and identified key taxa associated with spoilage during ambient temperature storage. Storage trials revealed that ‘Jingcang 1’ cultivar exhibits poor storability, characterized by rapid color change and early onset of decay. High-throughput sequencing analysis demonstrated that alterations in composition and structure of the fungal communities were more pronounced than those of bacterial communities. Both fungal diversity and richness fluctuated throughout the decay stages, and these shifts were strongly associated with specific key microbial genera, indicating their potential importance in community succession. Multiple approaches, including linear discriminant analysis effect size (LEfSe), SPEC-OCCU, and co-occurrence network analysis, consistently identified Aspergillus as a key biomarker genus. A total of 47 isolates were obtained from decayed tissue via pure culture methods. Phylogenetic analysis of their ITS sequences classified all isolates into 13 Aspergillus species, a result consistent with the microbiome data. In vivo pathogenicity assays confirmed that all 13 species were pathogenic to jujube fruit, albeit with varying levels of virulence. Notably, three species, A. piperis, A. luchuensis and A. aflatoxiformans, are newly reported here as causal agents of jujube decay. Our findings elucidate the dynamics of the microbial ecosystem during jujube fruit decay and provide a critical foundation for developing safe, effective, and targeted biocontrol strategies.
Disciplines :
Biotechnology
Author, co-author :
Wang, Jian-Yu; Shandong Institute of Pomology, Shandong, China
Jiao, Ke-Xin; College of Life Sciences, Shandong Agricultural University, Shandong, China
Mao, Min-Xin; Shandong Institute of Pomology, Shandong, China
Li, Cheng-Gang; Shandong University of Traditional Chinese Medicine, Shandong, China
Qu, Jianping ; Université de Liège - ULiège > TERRA Research Centre > Entomologie, Phytopathologie et Productions Innovantes (EPPI) ; College of Life Sciences, Shandong Agricultural University, Shandong, China
Zhou, Bo; College of Life Sciences, Shandong Agricultural University, Shandong, China
Zhang, Qian; Shandong Institute of Pomology, Shandong, China ; Jujube Industry Research Institute of Maigaiti County, Kashgar, China
Hao, Qing; Research Institute of Fruit and Vegetable, Xinjiang Academy of Agricultural Sciences, Urumqi, China ; Jujube Industry Research Institute of Maigaiti County, Kashgar, China
Language :
English
Title :
Fungal community succession drives the decay of jujube fruit (Ziziphus jujuba Mill. cv. Jingcang 1) during ambient storage
This work was supported by the Kashgar Science and Technology Plan ( KS2024042 ); the Agriculture Research System of China (CARS-30); the Shandong Provincial Natural Science Foundation ( ZR2025QC301 ); the Earmarked Fund of Xinjiang Jujube Industrial Technology System ( XJLGCYJSTX02 ); the Youth Engineering Project of Shandong Institute of Pomology ( 2023GSKY06 ).
Abdelfattah, A., Malacrinò, A., Wisniewski, M., Cacciola, S.O., Schena, L., 2018. Metabarcoding: a powerful tool to investigate microbial communities and shape future plant protection strategies. Biol. Control 120, 1-10. https://doi.org/10.1016/j.biocontrol.2017.07.009.
Banerjee, S., Zhao, C., Kirkby, C.A., Coggins, S., Zhao, S., Bissett, A., van der Heijden, M.G.A., Kirkegaard, J.A., Richardson, A.E., 2021. Microbial interkingdom associations across soil depths reveal network connectivity and keystone taxa linked to soil fine-fraction carbon content. Agr. Ecosyst. Environ. 320, 107559. https://doi.org/10.1016/j.agee.2021.107559.
Børve, J., Stensvand, A., 2015. Factors affecting postharvest fungal fruit decay in sweet cherry in a cool, wet climate. Acta Hortic. 1079, 307-312. https://doi.org/10.17660/ActaHortic.2015.1079.37.
Calvo, H., Mendiara, I., Arias, E., Gracia, A.P., Blanco, D., Venturini, M.E., 2020. Antifungal activity of the volatile organic compounds produced by Bacillus velezensis strains against postharvest fungal pathogens. Postharvest Biol. Tec. 111208. https://doi.org/10.1016/j.postharvbio.2020.111208.
Dai, K., Han, P., Zou, X., Jiang, S., Xu, F., Wang, H., Wei, Y., Shao, X., 2021. Hot air treatment reduces postharvest decay in Chinese bayberries during storage by affecting fungal community composition. Food Res. Int. 140, 110021. https://doi.org/10.1016/j.foodres.2020.110021.
Ding, Y., Wei, R., Wang, L., Yang, C., Li, H., Wang, H., 2021. Diversity and dynamics of microbial ecosystem on berry surface during the ripening of Ecolly (Vitis vinifera L.) grape in Wuhai, China. World J. Microb. Biot. 37, 214. https://doi.org/10.1007/s11274-021-03170-8.
Diskin, S., Feygenberg, O., Maurer, D., Droby, S., Prusky, D., Alkan, N., 2017. Microbiome alterations are correlated with occurrence of postharvest stem-end rot in mango fruit. Phytobiomes J. 1 (3), 117-127. https://doi.org/10.1094/PBIOMES-05-17-0022-R.
Dong, C., Wang, L., Li, Q., Shang, Q., 2021. Epiphytic and endophytic fungal communities of tomato plants. Hortic. Plant J. 7 (1), 38-48. https://doi.org/10.1016/j.hpj.2020.09.002.
Droby, S., Wisniewski, M., 2018. The fruit microbiome: a new frontier for postharvest biocontrol and postharvest biology. Postharvest Biol. Tec. 140, 107-112. https://doi.org/10.1016/j.postharvbio.2018.03.004.
Fontaine, K., Fourrier-Jeandel, C., Armitage, A.D., Boutigny, A., Crépet, M., Caffier, V., Gnide, D.C., Shiller, J., Le Cam, B., Giraud, M., Ioos, R., Aguayo, J., 2021. Identification and pathogenicity of Alternaria species associated with leaf blotch disease and premature defoliation in French apple orchards. PeerJ 9, e12496. https://doi.org/10.7717/peerj.12496.
Fresno, D.H., Munné-Bosch, S., 2021. Differential tissue-specific jasmonic acid, salicylic acid, and abscisic acid dynamics in sweet cherry development and their implications in fruit-microbe interactions. Front. Plant Sci. 12. https://doi.org/10.3389/fpls.2021.640601.
Gao, C., Zhang, Y., Li, H., Gao, Q., Cheng, Y., Ogunyemi, S.O., Guan, J., 2022. Fruit bagging reduces the postharvest decay and alters the diversity of fruit surface fungal community in ‘Yali’ pear. BMC Microbiol. 22, 239. https://doi.org/10.1186/s12866-022-02653-4.
Gao, Q., Zhang, Y., Gao, C., Li, H., Cheng, Y., Qian, X., Zhang, L., Liu, J., Ogunyemi, S.O., Guan, J., 2023. The microbial diversity in relation to postharvest quality and decay: organic vs. conventional pear fruit. Foods 12 (10), 1980. https://doi.org/10.3390/foods12101980.
Ge, Y., Chen, Y., Li, C., Wei, M., Lv, J., Meng, K., 2017. Inhibitory effects of sodium silicate on the fungal growth and secretion of cell wall-degrading enzymes by Trichothecium roseum. J. Phytopathol. 165 (9), 620-625. https://doi.org/10.1111/jph.12600.
Geng, C., Liu, X., Ma, J., Ban, H., Bian, H., Huang, G., 2023. High strength, controlled release of curcumin-loaded ZIF-8/chitosan/zein film with excellence gas barrier and antibacterial activity for litchi preservation. Carbohydr. Polym. 306, 120612. https://doi.org/10.1016/j.carbpol.2023.120612.
González-Curbelo, M.Á., Kabak, B., 2023. Occurrence of mycotoxins in dried fruits worldwide, with a focus on aflatoxins and ochratoxin a: a review. Toxins 15 (9), 576. https://doi.org/10.3390/toxins15090576.
Gweon, H.S., Bowes, M.J., Moorhouse, H.L., Oliver, A.E., Bailey, M.J., Acreman, M.C., Read, D.S., 2021. Contrasting community assembly processes structure lotic bacteria metacommunities along the river continuum. Environ. Microbiol. 23 (1), 484-498. https://doi.org/10.1111/1462-2920.15337.
Harteveld, D.O.C., Akinsanmi, O.A., Drenth, A., 2014. Pathogenic variation of Alternaria species associated with leaf blotch and fruit spot of apple in Australia. Eur. J. Plant Pathol. 139 (4), 789-799. https://doi.org/10.1007/s10658-014-0433-6.
Hou, D., Wang, C., Yang, Y., Jing, S., Zhu, B., Xu, H., Kou, L., 2024. Effects of transport vibration on storage quality and expression of genes related to cell wall metabolism of winter jujube (Zizyphus jujuba Mill. Cv. Dalidongzao). Postharvest Biol. Technol. 209, 112729. https://doi.org/10.1016/j.postharvbio.2023.112729.
Huang, K., Sun, X., Li, X., Huang, X., Sun, Z., Li, W., Wang, J., Tian, D., Lin, C., Wu, X., Miao, C., Li, Y., Xu, P., Fan, T., Zhu, S., Li, N., Zeng, L., Liu, J., Sui, Y., 2023. Pathogenic fungi shape the fungal community, network complexity, and pathogenesis in kiwifruit. Microb. Biotechnol. 16 (12), 2264-2277. https://doi.org/10.1111/1751-7915.14344.
Janisiewicz, W.J., Buyer, J.S., 2010. Culturable bacterial microflora associated with nectarine fruit and their potential for control of brown rot. Can. J. Microbiol. 56, 480-486. https://doi.org/10.1139/W10-031.
Kusstatscher, P., Cernava, T., Abdelfattah, A., Gokul, J., Korsten, L., Berg, G., 2020. Microbiome approaches provide the key to biologically control postharvest pathogens and storability of fruits and vegetables. FEMS Microbiol. Ecol. 96 (7), 1. https://doi.org/10.1093/femsec/fiaa119.
Lei, X., Liu, Y., Guo, Y., Wang, W., Zhang, H., Yi, L., Zeng, K., 2022. Debaryomyces nepalensis reduces fungal decay by affecting the postharvest microbiome during jujube storage. Int. J. Food Microbiol. 379, 109866. https://doi.org/10.1016/j.ijfoodmicro.2022.109866.
Liu, M., Wang, J., Wang, L., Liu, P., Zhao, J., Zhao, Z., Yao, S., Stanica, F., Liu, Z., Wang, L., Ao, C., Dai, L., Li, X., Zhao, X., Jia, C., 2020. The historical and current research progress on jujube-a superfruit for the future. Hortic. Res. 7, 119. https://doi.org/10.1038/s41438-020-00346-5.
Liu, Y., Lei, X., Deng, B., Chen, O., Deng, L., Zeng, K., 2022. Methionine enhances disease resistance of jujube fruit against postharvest black spot rot by activating lignin biosynthesis. Postharvest Biol. Technol. 190, 111935. https://doi.org/10.1016/j.postharvbio.2022.111935.
Madbouly, A.K., Abo Elyousr, K.A.M., Ismail, I.M., 2020. Biocontrol of Monilinia fructigena, causal agent of brown rot of apple fruit, by using endophytic yeasts. Biol. Control 144, 104239. https://doi.org/10.1016/j.biocontrol.2020.104239.
Mo, J., Rashwan, A.K., Osman, A.I., Eletmany, M.R., Chen, W., 2024. Potential of Chinese bayberry (Myrica rubra Sieb. et Zucc.) fruit, kernel, and pomace as promising functional ingredients for the development of food products: a comprehensive review. Food Bioprocess Technol. 17 (11), 3506-3524. https://doi.org/10.1007/s11947-023-03313-9.
Nikkhah, M., Hashemi, M., 2020. Boosting antifungal effect of essential oils using combination approach as an efficient strategy to control postharvest spoilage and preserving the jujube fruit quality. Postharvest Biol. Technol. 164, 111159. https://doi.org/10.1016/j.postharvbio.2020.111159.
Qin, G.Z., Tian, S.P., 2004. Biocontrol of postharvest diseases of jujube fruit by Cryptococcus laurentii combined with a low dosage of fungicides under different storage conditions. Plant Dis. 88 (5), 497-501. https://doi.org/10.1094/PDIS.2004.88.5.497.
Rehman, S., Aslam, H., Ahmad, A., Khan, S.A., Sohail, M., 2014. Production of plant cell wall degrading enzymes by monoculture and co-culture of Aspergillus niger and Aspergillus terreus under SSF of banana peels. Braz. J. Microbiol. 45 (4), 1485-1492. https://doi.org/10.1590/S1517-83822014000400045.
Schnürer, J., Olsson, J., Börjesson, T., 1999. Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet. Biol. 27, 209-217. https://doi.org/10.1006/fgbi.1999.1139.
Shi, W., Dong, Q., Saleem, M., Wu, X., Wang, N., Ding, S., Huang, J., Wang, X., Zhou, B., Gao, Z., 2022. Microbial-based detonation and processing of vegetable waste for high quality compost production at low temperatures. J. Clean. Prod. 369, 133276. https://doi.org/10.1016/j.jclepro.2022.133276.
Shi, W., Su, G., Li, M., Wang, B., Lin, R., Yang, Y., Wei, T., Zhou, B., Gao, Z., 2021. Distribution of bacterial endophytes in the non-lesion tissues of potato and their response to potato common scab. Front. Microbiol. 12, 616013. https://doi.org/10.3389/fmicb.2021.616013.
Sohail, M., Ahmad, A., Khan, S.A., 2016. Production of cellulase from Aspergillus terreus MS105 on crude and commercially purified substrates. 3 Biotech 6 (1). https://doi.org/10.1007/s13205-016-0420-z.
Sunpapao, A., Suwannarach, N., Kumla, J., Dumhai, R., Riangwong, K., Sanguansub, S., Wanchana, S., Arikit, S., 2022. Morphological and molecular identification of plant pathogenic fungi associated with dirty panicle disease in coconuts (Cocos nucifera) in Thailand. J. Fungi 8, 335. https://doi.org/10.3390/jof8040335.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. https://doi.org/10.1093/molbev/mst197.
Thammachote, N., Sripong, K., Uthairatanakij, A., Laohakunjit, N., Limmatvapirat, S., Ma, G., Zhang, L., Kato, M., Jitareerat, P., 2023. Influence of silver nanoparticles on postharvest disease, pericarp hardening, and quality of mangosteen. Postharvest Biol. Technol. 204, 112470. https://doi.org/10.1016/j.postharvbio.2023.112470.
Udoh, I.P., Eleazar, C.I., Ogeneh, B.O., Ohanu, M.E., 2015. Studies on fungi responsible for the spoilage/deterioration of some edible fruits and vegetables. Adv. Microbiol. 5, 285-290. https://doi.org/10.4236/aim.2015.54027.
Vicente-Díez, I., Moreira, X., Pastor, V., Vilanova, M., Pou, A., Campos-Herrera, R., 2023. Control of post-harvest gray mold (Botrytis cinerea) on grape (Vitis vinifera) and tomato (Solanum lycopersicum) using volatile organic compounds produced by Xenorhabdus nematophila and Photorhabdus laumondii subsp. Laumondii. Biocontrol 68, 549-563. https://doi.org/10.1007/s10526-023-10212-7.
Wisniewski, M., Droby, S., 2019. The postharvest microbiome: The other half of sustainability. Biol. Control 137, 104025. https://doi.org/10.1016/j.biocontrol.2019.104025.
Xiao, X.E., Wang, W., Crous, P.W., Wang, H.K., Jiao, C., Huang, F., Pu, Z.X., Zhu, Z.R., Li, H.Y., 2021. Species of Botryosphaeriaceae associated with citrus branch diseases in China. Persoonia 47 (1), 106-135. https://doi.org/10.3767/persoonia.2021.47.03.
Zhang, C., Gao, Z., Shi, W., Li, L., Tian, R., Huang, J., Lin, R., Wang, B., Zhou, B., 2020. Material conversion, microbial community composition and metabolic functional succession during green soybean hull composting. Bioresource Technol. 316, 123823. https://doi.org/10.1016/j.biortech.2020.123823.
Zhang, Q., Shi, W., Zhou, B., Du, H., Xi, L., Zou, M., Zou, H., Xin, L., Gao, Z., Chen, Y., 2021. Variable characteristics of microbial communities on the surface of sweet cherries under different storage conditions. Postharvest Biol. Technol. 173, 111408. https://doi.org/10.1016/j.postharvbio.2020.111408.
Zhang, S., Zheng, Q., Xu, B., Liu, J., 2019. Identification of the fungal pathogens of postharvest disease on peach fruits and the control mechanisms of Bacillus subtilis JK-14. Toxins 11 (6), 322. https://doi.org/10.3390/toxins11060322.
Zhang, Y., Mahidul Islam Masum, M., Gao, C., Cheng, Y., Guan, J., 2022. Ozone reduces the fruit decay of postharvest winter jujube by altering the microbial community structure on fruit surface. Microbiol. Res. 262, 127110. https://doi.org/10.1016/j.micres.2022.127110.
Zhao, Q., Shi, Y., Legrand Ngolong Ngea, G., Zhang, X., Yang, Q., Zhang, Q., Xu, X., Zhang, H., 2023. Changes of the microbial community in kiwifruit during storage after postharvest application of Wickerhamomyces anomalus. Food Chem. 404, 134593. https://doi.org/10.1016/j.foodchem.2022.134593.
Zhimo, V.Y., Kumar, A., Biasi, A., Abdelfattah, A., Sharma, V.K., Salim, S., Feygenberg, O., Bartuv, R., Freilich, S., Whitehead, S.R., Wisniewski, M., Droby, S., 2022. Assembly and dynamics of the apple carposphere microbiome during fruit development and storage. Front. Microbiol. 13, 928888. https://doi.org/10.3389/fmicb.2022.928888.
Zhu, C., Lin, Y., Wang, Z., Luo, W., Zhang, Y., Chu, C., 2023. Community assembly and network structure of epiphytic and endophytic phyllosphere fungi in a subtropical mangrove ecosystem. Front. Microbiol. 14. https://doi.org/10.3389/fmicb.2023.1147285.