Fruit Bagging Reduces The Postharvest Decay and Al
Fruit Bagging Reduces The Postharvest Decay and Al
Fruit Bagging Reduces The Postharvest Decay and Al
Abstract
Background: Fruit bagging is an effective technique for fruit protection in the orchard management. Bagging can
create a micro-environment for fruit growth and affect fruit quality during storage, in which the diversity of micro-
organisms may play an important role. Therefore, various methods including biochemistry, analytical chemistry, and
bioinformatics methods were used to reveal the influences of fruit bagging on postharvest fruit quality, physiological
characters, decay and surface fungal community of ‘Yali’ pear fruit were investigated in this study.
Results: Fruit bagging significantly decreased the postharvest decay after 15 days of ambient storage. There were
no significant differences in fruit firmness, titratable acid and ethylene production rate between the fruit-bagging
and non-bagging group after 15 days of storage, while the soluble solids contents (SSC) and respiration rate in non-
bagging fruit was significantly higher than that in fruit-bagging after 15 days of storage. Furthermore, the surface
microbes of pear were collected and determined by the new generation sequencing technology. The alpha diversity
of fungi in non-bagging fruit decreased significantly after 15 days of storage, while there were no significant changes
in bagging fruit. Ascomycota and Basidiomycota were the two major phyla detected in the bagging fruit, and the
dominant fungal genera were Alternaria (23.7%), Mycosphaerella (17.25%), Vishniacozyma (16.14%), and Aureoba-
sidium (10.51%) after 15 days of storage. For the non-bagging pear, Ascomycota was the only phylum detected, and
the dominant genera was Pichia (83.32%) after 15 days of storage. The abundance of Pichia may be regarded as the
biomarker to indicate the degree of fruit decay.
Conclusions: This study showed that fruit bagging could significantly reduce postharvest fruit decay and respiration
rate of ‘Yali’ pear. Significant differences were found in fungal composition between bagging and non-bagging pear
after storage for 0 or 15 days. Fruit bagging maintained the diversity of fungi on the fruit surface, increased the abun-
dance of non-pathogenic fungi, and even antagonistic fungi such as Aureobasidium, Vishniacozyma, and Mycosphaere-
lla. A reduction in the abundance of pathogenic fungi and incidence of postharvest decay during the storage of ‘Yali’
pear were also recorded. In conclusion, fruit-bagging changed the fungal diversity on fruit surface of ‘Yali’ pear, which
had significant effect on reducing postharvest fruit decay, and thus prolong the storage period of ‘Yali’ pears. The
†
Congcong Gao and Yang Zhang share equal contribution.
*Correspondence: [email protected]
1
Institute of Biotechnology and Food Science, Hebei Academy of Agriculture
and Forestry Sciences, Shijiazhuang 050051, China
Full list of author information is available at the end of the article
© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the
original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or
other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this
licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativeco
mmons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Gao et al. BMC Microbiology (2022) 22:239 Page 2 of 12
future thrust of this study will focus on the isolation of fungi or bacteria from pear fruit surface and identify their roles
in causing fruit decay and changing fruit quality during storage.
Keywords: Postharvest decay, Fruit bagging, Fungal community, ‘Yali’ pear, Pichia
Fig. 2 Effects of fruit bagging on firmness (A), soluble solids content (B) and titratable acid content (C) of ‘Yali’ pear. B: bagging; NB: non-bagging
Fig. 3 Effects of fruit bagging on respiration rate (A) and ethylene production rate (B) of ‘Yali’ pear during storage at ambient temperature. B:
bagging; NB: non-bagging
higher than that of bagging fruit after 5 days of storage, Beta diversity analysis
and reached the level of bagging fruit after 10 days of According to the results of beta diversity, the bagging
storage (Fig. 3B). (B0) and non-bagging groups (NB0) at the beginning of
storage could be clearly separated on PCoA2, indicating
that fruit bagging significantly affected the fungal com-
Fruit bagging changed fungal diversity on the surface munity on the surface of pear at harvest (Fig. 5). After
of pear fruit 15 days of storage, fruit bagging (B15) and non-bag-
Alpha diversity analysis ging (NB15) group could also be clearly differentiated
Five indexes, including Chao1, Good’s coverage, Shan- on PCoA1, indicating that fruit bagging significantly
non, Pielou, and Observed species, were used to show affected the fungal community on the surface after
the effect of bagging on the alpha diversity of fungal storage. However, bagging fruit after 15 days of storage
community on fruit surface. The results showed that (B15) could not be clearly differentiated in PCoA1 or
the diversity and richness of fungal species on the sur- PCoA2 from 0 day of storage (B0), while non-bagging
face of non-bagging fruit were significantly higher than fruit after 15 days of storage (NB15) could be clearly dif-
that on the surface of bagging fruit at harvest (Fig. 4). ferentiated in PCoA1 from 0 day of storage (NB0). This
The surface fungal diversity of non-bagging fruit result indicates that bagging treatment could maintain
decreased significantly, while there was no significant the fungal diversity on fruit surface of ‘Yali’ pear.
change in bagging fruit after storage for 15 days.
Gao et al. BMC Microbiology (2022) 22:239 Page 5 of 12
Fig. 4 Alpha diversity of fungal community on surface of ‘Yali’ pear. Chao1 and Observed species index indicate the richness of fungal community;
Shannon index represents the fungal diversity; Pielou was used to characterize evenness of fungal community; Good’s Coverage indicates the
amount of determined species. B: bagging; NB: non-bagging
Fungal composition on the surface of pear fruit Exobasidiomycetes (8.8%), and Agaricomycetes (3.9%).
The main fungal composition on pear fruit surface at The most abundant genera were Mycosphaerella (30.3%),
phyla, class, order, family and genus level was shown in Papiliotrema (15%), Aureobasidium (7.4%), Vishniaco-
Fig. 6. At the initial storage stage of the bagging group, zyma (9.6%), Golubevia (8%), and Acremonium (1.6%).
Ascomycota (72%) and Basidiomycota (25%) were the After 15 days of storage, Ascomycota (96%), Saccharo-
dominant phyla, and the main classes were Dothideo- mycetes (95%), Saccharomycetates (95.4%), Pichiaceae
mycetes (68%), Tremellomycetes (22%), Sordariomycetes (83.5%), and Pichia (83.3%) were the dominant phyla,
(3.5%), and Exobasidiomycetes (2.5%). The most abundant class, order, family and genus in the non-bagging group,
fungal genera were Alternaria (38.2%), Aureobasidium respectively. On the other hand, the fungal composition
(16%), Vishniacozyma (18.2%), Mycosphaerella (12.5%), on the surface of bagging fruit was much more diverse.
Acremonium (3%), Papiliotrema (2.2%), and Golubevia Ascomycota (57%), and Basidiomycota (42%) were the
(2.1%). Ascomycota (49%), and Basidiomycota (39%) were dominant phyla. Dothideomycetes (52%), Tremellomy-
the dominant phyla in the non-bagging group at the ini- cetes (20%), Exobasidiomycetes (21%), and Sordariomy-
tial storage stage. The main classes were Dothideomycetes cetes (3.8%) were the main classes. Hypocreales (3.7%),
(40%), Tremellomycetes (26%), Sordariomycetes (5.7%), Exobasidiales (11.4%), Golubeviales (9.8%), Dothideates
Gao et al. BMC Microbiology (2022) 22:239 Page 6 of 12
Fig. 5 Beta diversity of fungal community on surface of bagging or non-bagging ‘Yali’ pear with 0 or 15 days of storage. B: bagging; NB:
non-bagging. The PERMANOVA (adonis) test was used for identifying the differences
(10.5%), Capnodiales (17.3%), Pleosporales (24.3%), degree of fruit decay, Pichia had the potential as a bio-
and Tremellales (19.3%) were the dominant orders. marker of fruit decay.
Cryptobasidiaceae (3.3%), Golubeviaceae (9.8%), Rhyn-
chogastremataceae (3%), Aureobasidiaceae (10.5%), Differences in the abundance of the yeast
Bulleribasidiaceae (16%), Mycosphaerellaceae (17.3%), Because the functions of yeast are complex and many of
and Pleosporaceae (23.7%) were the dominant fami- them act as healthy fungi antagonizing pathogens, the
lies. Acaromyces (3.3%), Acremonium (3%), Meira (8%), differences in the abundance of yeast between differ-
Golubevia (9.8%), Papiliotrema (3%), Aureobasidium ent groups were analyzed. As shown in Fig. 8, the rela-
(10.5%), Vishniacozyma (16%), Mycosphaerella (17.2%), tive abundance of Pichia was significantly higher in NB15
and Alternaria (23.7%) were the main genera. than other groups, while yeasts including Vishniacozyma,
Aureobasidium, and Golubevia showed significant higher
Biomarker identification by LEfSe abundance in B15 than other groups. Hence, indicat-
Linear discriminant analysis effect size (LEfSe) was used ing they might play positive roles in healthy fruit. On
to analyze the fungal biomarkers on the surface of pear the other hand, the abundance of fungi including Meira,
different groups. As shown in Fig. 7, biomarkers in all Acaromyces, and Papiliotrema showed no significant dif-
groups at different taxonomic levels were identified. ferences between groups.
Alernaria, Vishniacozyma, and Aureobasidium can be
regarded as the biomarkers of B0 group. There are also Correlation analysis of postharvest fruit decay
three fungal genera that can be used as biomarkers in the and microbial diversity
NB0 group: Mycosphaerella, Papiliotrema, and Nigros- The canonical correspondence analysis (CCA) was
pora. Five fungal genera including Golubvia, Meira, Acre- performed to show the relationships of bagging, stor-
monium, Acaromyces, and Simplicillium were identified age time, microbial diversity, and fruit qualities. Given
as biomarkers for the B15 group. The biomarker of NB15 that fruit firmness, respiration rate, and decay index
group was Pichia. Since the NB15 group had the highest were significantly affected by bagging, they were used
Gao et al. BMC Microbiology (2022) 22:239 Page 7 of 12
Fig. 6 Fungal composition on surface of ‘Yali’ pear at phyla (A), class (B), order (C), family (D) and genus (E) level. B: bagging; NB: non-bagging
Fig. 7 Fungal biomarkers on the surface of pear of different groups by linear discriminant analysis effect size (LEfSe). A: Histogram of LDA value
distribution. B: Taxonomic cladogram. The threshold of linear discriminant analysis was set as 4. B: bagging; NB: non-bagging
Gao et al. BMC Microbiology (2022) 22:239 Page 9 of 12
Fig. 8 Differences in the abundance of yeasts between bagging and non-bagging groups in ‘Yali’ pear
storage, which may be due to the little variations in tem- community does not change drastically due to environ-
perature and relative humidity after bagging [19, 20]. The mental changes. In addition, abamectin was used after
micro-environment inside fruit bag is controlled, hence, fruit bagging. Although no effect of abamectin on phyl-
microbial competition is relatively harmonious, and the lospheric fungi was found, it however, significantly affect
Gao et al. BMC Microbiology (2022) 22:239 Page 10 of 12
Fig. 9 Correlation of postharvest fruit decay and microbial diversity by canonical correspondence analysis in ‘Yali’ pear. DI: Decay index. RR:
Respiratory rate. B: bagging; NB: non-bagging
bacterial diversity [21]. The effect of pesticides on fungal such as leaf spot, leaf litter, and branch blight [29–32]. In
diversity of fruit surface in non-bagging pear should be addition, Mycosphaerella sp. has been reported to be the
noticed. Therefore, the decrease of fungal diversity on causal organism of pear skin stain which had a stronger
fruit surface of non-bagging pear was probably resulted pathogenicity than Penicillium spp. and Alternaria spp.
by the use of abamectin as well. Most of the pathogens [33]. Pichia was found to be the dominant genus in the
colonize the fruit surface in the form of latent infection non-bagging group after storage for 15 days. Pichia has
and will not cause disease in the short term, thus main- been reported to have a negative impact on the growth of
taining the diversity of fungal community on the fruit Zygosaccharomyces spp., Botrytis cinerea, and Brettano-
surface. It was found that bagging significantly reduced myces bruxellensis, and it could secrete toxins or organic
postharvest decay after storage for 15 days, and the fun- acids, which were lethal to other yeasts and filamentous
gal diversity of bagging group was higher than that of fungi [34–37]. These characteristics therefore, gave it an
non-bagging group. Thus, indicating that the dominant advantage to become the dominant species by negatively
strains that appeared were associated with fruit decay. affecting the growth of other fungi.
Fungal composition on the surface of pear fruit showed Bagging helped to maintain the fungal diversity on
that the main fungi on the surface of pear were Ascomy- the fruit surface of ‘Yali’ pear after storage for 15 days.
cota, which grow fast and can survive harsh conditions In addition to common pathogenic fungi such as Alter-
with low nutrient level [22]. They can adapt to a wide naria, Mycosphaerella, and Acremonium [38–41]. A
range of substrates in challenging environments such as number of yeast or yeast-like fungi including Vishniaco-
ultraviolet light, water and high temperature stress [23]. zyma, Aureobasidium, Papiliotrema, Golubevia, Meira,
Ascomycota has been shown to be pathogenic fungi in and Acaromyces, which have been reported to have a
plants and insects [24]. However, Mycosphaerella was variety of functions were also observed in this study.
dominant in non-bagging group at the beginning of the Vishniacozyma was reported to have an inhibitory effect
storage period which was significantly different from the on Penicillium, which can control blue mold in apple,
bagging group. Mycosphaerella is widely distributed on and is widely existed [42, 43]. Aureobasidium was also
trees, herbaceous plants, and cultivated crops such as reported for its effectiveness against blue mold caused by
saprophytes, plant pathogens, or endophytes [25–28]. It Penicillium expansum in stored apple fruit, and can be
has been reported Mycosphaerella can cause leaf diseases found in a variety of environments and with a worldwide
Gao et al. BMC Microbiology (2022) 22:239 Page 11 of 12
distribution from cold to warm climates [44, 45]. Papili- HL, QG, and YC. Writing-review & editing-preparation: SOO. All authors read
and approved the final manuscript.
otrema was found to be present in plant leaves which
was non-pathogenic, producing β-galactosidase [46, 47]. Funding
Golubevia has been found to regulate the plant defense We appreciate the financial assistance provided from the Agriculture Science
and Technology Innovation Project of Hebei Academy of Agriculture and For-
system and has certain antagonistic effect on powdery estry Sciences (HAAFS, 2019-2-1), the Hebei Postdoctoral Science Foundation
mildew of cucumber [48]. Acaromyces and Meira was (B2021003034), and the Talents Construction Project of Science and Technol-
reported to be the pathogens causing fruit stain of Japa- ogy Innovation of HAAFS (C21R1303).
nese pear [49]. Result from this study has shown that Availability of data and materials
the abundance of Vishniacozyma, Aureobasidium, and Data of ITS amplicon sequencing of the samples were submitted to NCBI
Golubevia, which have been reported to have antagonis- under the Bioproject ID PRJNA835258.
tic effects, were significantly higher in B15 than NB15.
The abundance of Vishniacozyma and Aureobasidium Declarations
were positively correlated with fruit firmness. Therefore, Ethics approval and consent to participate
Vishniacozyma and Aureobasidium were supposed to be All methods were performed in accordance with the relevant guidelines and
regarded as the healthy fungi after fruit bagging. regulations. Permission was obtained for collection of the plant sample and
conducting experiment in Zhaoxian orchard Shijiazhuang.
Previous results have shown that fruit bagging signifi-
cantly increased fungal diversity and promote healthy Consent for publication
fungal communities which protect fruit from the inva- Not applicable.
sion of pathogens [50]. This report [50] is however, con- Competing interests
sistent with the results of this study. Therefore, fruit The authors declare that they have no conflicts of interest concerning this
bagging has generated a diverse fungal community on the article.
fruit surface of pear, in which antagonistic yeasts were Author details
relatively abundant, which may be involved in inhibiting 1
Institute of Biotechnology and Food Science, Hebei Academy of Agriculture
the reproduction of pathogens and reducing the occur- and Forestry Sciences, Shijiazhuang 050051, China. 2 Plant Genetic Engineering
Center of Hebei Province, Shijiazhuang 050051, China. 3 State Key Laboratory
rence of postharvest decay. of Rice Biology, Ministry of Agriculture Key Lab of Molecular Biology of Crop
Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hang-
zhou 310013, China.
Conclusions Received: 6 May 2022 Accepted: 23 September 2022
This study showed that fruit bagging could significantly
reduce postharvest fruit decay and respiration rate of
‘Yali’ pear, and affect other fruit qualities and physiologi-
cal characteristics. The richness, evenness, and diversity References
of the fungal community on pear surface were higher in 1. Chen JL, Yan S, Feng Z, Xiao L, Hu XS. Changes in the volatile com-
pounds and chemical and physical properties of Yali pear (Pyrus
bagging group than in non-bagging one, and significant
bertschneideri Reld) during storage. Food Chem. 2006;97:248–55.
differences were found in fungal composition between 2. Zhang J, Jiang L, Sun C, Jin L, Lin M, Huang Y, et al. Indole-3-acetic acid
bagging and non-bagging pear after storage for 0 or inhibits blue mold rot by inducing resistance in pear fruit wounds. Sci
Hortic. 2018;231:227–32.
15 days. Hence, fruit bagging maintained the diversity
3. Oyom W, Li Y-C, Prusky D, Zhang Z, Bi Y, Tahergorabi R. Recent advances
of fungi on the fruit surface, increased the abundance of in postharvest technology of Asia pears fungi disease control: A review.
non-pathogenic fungi, including antagonistic fungi such Physiol Mol Plant Pathol. 2022;117:101771.
4. Cao J, Jiang W. Induction of resistance in Yali pear (Pyrus bretschneideri
as Aureobasidium, Vishniacozyma, and Mycosphaere-
Rehd.) fruit against postharvest diseases by acibenzolar-S-methyl
lla. In addition, it consequently reduced the abundance sprays on trees during fruit growth. Sci Hortic. 2006;110:181–6.
of pathogenic fungi and incidence of postharvest decay 5. Zheng X, Yu T, Chen R, Huang B, Wu CH. Inhibiting Penicillium expan-
sum infection on pear fruit by Cryptococcus laurentii and cytokinin.
during the storage of ‘Yali’ pear. The future thrust of this
Postharvest Biol Technol. 2007;45:221–7.
study will focus on the isolation of fungi or bacteria from 6. Ewekeye T, Oke O, Esan O. Studies on post harvest rot of apple (Malus
pear fruit surface and identify their roles in causing fruit domestica Borkh). Indian J Plant Sci. 2016;5:36–41.
7. Ostry V. Alternaria mycotoxins: an overview of chemical characteriza-
decay and changes in fruit quality during storage.
tion, producers, toxicity, analysis and occurrence in foodstuffs. World
Mycotoxin J. 2008;1:175–88.
Acknowledgements
8. Zain ME. Impact of mycotoxins on humans and animals. J Saudi Chem
We thank Mr. Wangwei Liang and Kunrui Hao from the Institute of Pear Sci-
Soc. 2011;15:129–44.
ence, Zhaoxian, Hebei for their assistance in orchard management.
9. Ali MM, Anwar R, Yousef AF, Li B, Luvisi A, De Bellis L, et al. Influence
of bagging on the development and quality of fruits. Plants (Basel).
Authors’ contributions
2021;10:358.
Conceptualization, writing-original draft preparation, and writing-review &
10. Feng Y, Cheng Y, He J, Li L, Guan J. Effects of 1-methylcyclopropene and
editing-preparation: CG, YZ, and JG. Analysis, investigation and methodology:
modified atmosphere packaging on fruit quality and superficial scald
in Yali pears during storage. J Integr Agric. 2018;17:1667–75.
Gao et al. BMC Microbiology (2022) 22:239 Page 12 of 12
11. Spadaro D, Droby S. Development of biocontrol products for posthar- chemical composition of apple wines produced from high-sugar juices. J
vest diseases of fruit: the importance of elucidating the mechanisms of Food Nutri Res. 2017;56:189–99.
action of yeast antagonists. Trends Food Sci Technol. 2016;47:39–49. 36. Mannazzu I, Domizio P, Carboni G, Zara S, Zara G, Comitini F, et al. Yeast
12. Khwantongyim P, Wansee S, Lu X, Zhang W, Sun G. Variations in the killer toxins: from ecological significance to application. Crit Rev Biotech-
community structure of fungal microbiota associated with apple fruit nol. 2019;39:603–17.
shaped by fruit bagging-based practice. J Fungi. 2021;7:764. 37. Zhang H, Wang L, Tan Y, Wang H, Yang F, Chen L, et al. Effect of Pichia on
13. Gao CC, Lin Q, Dong CH, Ji HP, Yu JZ, Chen CK, et al. Effects of ozone shaping the fermentation microbial community of sauce-flavor Baijiu. Int
concentration on the postharvest quality and microbial diversity of J Food Microbiol. 2021;336:108898.
Muscat Hamburg grapes. RSC Adv. 2020;10:9037–45. 38. Hou Y, Zhang X, Zhang N, Naklumpa W, Zhao W, Liang X, et al. Genera
14. Zhang Q, Shi W, Zhou B, Du H, Chen Y. Variable characteristics of micro- Acremonium and Sarocladium cause brown spot on bagged apple fruit in
bial communities on the surface of sweet cherries under different China. Plant Dis. 2019;103:1889–901.
storage conditions. Postharvest Biol Technol. 2020;173:111408. 39. Khosla K, Gupta A. First report of Acremonium kiliense causing fruit rot of
15. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, pears in India. New Disease Reports. 2016;33:14–4.
et al. Reproducible, interactive, scalable and extensible microbiome 40. Wang P-H, Wu P-C, Huang R, Chung K-R. The role of a nascent polypep-
data science using QIIME 2. Nat Biotechnol. 2019;37:1091. tide-associated complex subunit alpha in siderophore biosynthesis,
16. Chen T, Liu Y-X, Huang L. ImageGP: An easy-to-use data visualization oxidative stress response, and virulence in Alternaria alternata. Mol Plant-
web server for scientific researchers iMeta, 2022;1:e5. Microbe Interact. 2020;33:668–79.
17. Sharma RR, Sanikommu VR. Preharvest fruit bagging for better protec- 41. Morgan-Jones G, Gams W, Notes on Hyphomycetes. XLI. An endophyte of
tion and postharvest quality of horticultural produce. In: Siddiqui MW, Festuca arundinacea and the anamorph of Epichloë typhina, new taxa in
editor. Preharvest modulation of postharvest fruit and vegetable qual- one of two new sections of Acremonium. Mycotaxon. 1982;15:311–8.
ity. New York: Academic Press; 2018. p. 455–89. 42. Félix CR, Andrade DA, Almeida JH, Navarro HMC, Fell JW, Landell MF.
18. Xia J, Zhang Z, Qu S, Xu C, Gao J. Effects of bagging on the quality Vishniacozyma alagoana sp nov a tremellomycetes yeast associ-
factors of Jiangsu red Fuji apple in the process of growth and develop- ated with plants from dry and rainfall tropical forests. Int J Syst Evol
ment. Jiangsu J Agricult Sci. 2009;25:351–6. Microbiol. 2020;70:3449–3454.
19. Dai P, Liang X, Wang Y, Gleason ML, Zhang R, Sun G. High humidity and 43. Ma Q, Shi Y, Li Z, Wang W, Sun P. Isolation and identification of Vishniacoz-
age-dependent fruit susceptibility promote development of Trichothe- yma carnescens PGLY-1 for the inhibition of pear green mold. China Fruits.
cium black spot on apple. Plant Dis. 2019;103:259–67. 2020;5:50–4.
20. Jiqiu W. Research progress on spotted-scar diseases of bagged apple 44. Bencheqroun SK, Bajji M, Massart B, Labhilili M, Jijakli S. In vitro and in
fruit. J Anhui Agric Sci. 2007;35:2941. situ study of postharvest apple blue mold biocontrol by Aureobasidium
21. Zhang BG, Tang L, Li ZM, Wang HL, Bai ZH. Effect of abamectin insec- pullulans: evidence for the involvement of competition for nutrients.
ticide on the microbial community in broccoli phyllosphere. Chin J Postharvest Biol Technol. 2007;46:128–35.
Environ Sci. 2009;30:1292–7. 45. Bozoudi D, Tsaltas D. The multiple and versatile roles of Aureobasidium
22. Challacombe JF, Hesse CN, Bramer LM, McCue LA, Lipton M, Purvine S, et al. pullulans in the vitivinicultural sector. Fermentation. 2018;4:85.
Genomes and secretomes of Ascomycota fungi reveal diverse functions in 46. Surussawadee J, Khunnamwong P, Srisuk N, Limtong S. Papiliotrema
plant biomass decomposition and pathogenesis. BMC Genomics. 2019;20:976. siamense fa, sp. nov., a yeast species isolated from plant leaves. Int J Syst
23. Jaber BM, Al-Silawi R, Al-Najjar T. Isolation and molecular identification Evol Microbiol. 2014;64:3058–3062.
of Ascomycetes in sediments and waters of the Gulf of Aqaba, Red Sea. 47. Ke Q, Fulmer P, Mizutani A. Toxicological evaluation of β-Galactosidase enzyme
Natural Science. 2012;4:555–61. produced by Papiliotrema terrestris. Regul Toxicol Pharmacol. 2018;92:213–9.
24. Muggia L, Ametrano CG, Sterflinger K, Tesei D. An overview of genomics, 48. Russ L, Lombaers-van der Plas C, Castillo-Russi JD, Zijlstra C, Köhl J.
phylogenomics and proteomics approaches in Ascomycota. Life. 2020;10:356. Deciphering the modes of action of Golubevia sp., an antagonist against
25. Verkley GJ, Starink-Willemse M. A phylogenetic study of some Septoria the causal agent of powdery mildew in wheat, using an mRNA-based
species pathogenic to Asteraceae based on ITS ribosomal DNA systems approach. Biol Control. 2021;152:104446.
sequences. Mycol Prog. 2004;3:315–23. 49. Yasuda F, Yamagishi D, Akamatsu H, Izawa H, Otani H. Fruit stain of
26. Crous PW, Groenewald JZ, Pongpanich K, Himaman W, Arzanlou Japanese pear caused by basidiomycetous, yeast-like fungi, Acaromyces
M, Wingfield MJ. Cryptic speciation and host specificity among ingoldii and Meira sp. Japan J Phytopathol. 2005;71:156–65.
Mycosphaerella spp. occurring on Australian Acacia species grown as 50. Amin M, Nasrin T, Alam SM, Reza M, Uddin M, Rahman M. Impact of pre-
exotics in the tropics. Stud Mycol. 2004;50:457–69. harvest fruit bagging and improved postharvest practices in reducing
27. Crous PW, Summerell BA, Carnegie AJ, Mohammed C, Himaman W, losses and managing quality of mango in the value chain system. Int J
Groenewald JZ. Foliicolous Mycosphaerella spp. and their anamorphs Postharvest Technol Innovation. 2019;6:117.
on Corymbia and Eucalyptus. Fungal Divers. 2007;26:143–85.
28. Park RF, Keane PJ, Wingfield MJ, Crous PW, Fungal diseases of eucalypt
foliage. In: Keane PJ, Kile GA, Podger FD, Brown BN, editors. Diseases and Publisher’s Note
pathogens of eucalypts. Australia: CSIRO Publishing; 2000. p. 153–239. Springer Nature remains neutral with regard to jurisdictional claims in pub-
29. Crous PW, Groenewald JZ, Mansilla JP, Hunter GC, Wingfield MJ. Phy- lished maps and institutional affiliations.
logenetic reassessment of Mycosphaerella spp. and their anamorphs
occurring on Eucalyptus. Stud Mycol. 2004;50:195–214.
30. Hunter GC, Crous PW, Wingfield BD, Pongpanich K, Wingfield MJ.
Ready to submit your research ? Choose BMC and benefit from:
Pseudocercospora flavomarginata sp. nov., from Eucalyptus leaves in
Thailand. Fungal Divers. 2006;22:71–90.
• fast, convenient online submission
31. Burgess TI, Barber PA, Sufaati S, Xu D, Hardy GSJ, Dell B. Mycosphaerella
spp. on Eucalyptus in Asia: new species, new hosts and new records. • thorough peer review by experienced researchers in your field
Fungal Divers. 2007;24:135–57. • rapid publication on acceptance
32. Carisse O, McNealis V. Development of action threshold to manage
• support for research data, including large and complex data types
common leaf spot and black seed disease of strawberry caused by
Mycosphaerella fragariae. Plant Dis. 2019;103:563–70. • gold Open Access which fosters wider collaboration and increased citations
33. Nam K-W, Oh S-Y, Yoon D-H. Pear skin stain caused by Mycosphaerella • maximum visibility for your research: over 100M website views per year
graminicola on Niitaka pear (Pyrus pyrifolia Nakai). Plant Pathol J. 2014;30:229.
34. Belda I, Ruiz J, Alonso A, Marquina D, Santos A. The biology of Pichia At BMC, research is always in progress.
membranifaciens killer toxins. Toxins. 2017;9:112.
35. Błaszczyk U, Sroka P, Satora P, Duliński R. Effect of Wickerhamomyces Learn more biomedcentral.com/submissions
anomalus and Pichia membranifaciens killer toxins on fermentation and