Next Article in Journal
Fungal Virus, FgHV1-Encoded p20 Suppresses RNA Silencing through Single-Strand Small RNA Binding
Previous Article in Journal
Deletion of the col-26 Transcription Factor Gene and a Point Mutation in the exo-1 F-Box Protein Gene Confer Sorbose Resistance in Neurospora crassa
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JoF
Volume 8
Issue 11
10.3390/jof8111170
jof-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Fusarium Species Associated with Maize Leaf Blight in Heilongjiang Province, China

by
Xi Xu
1,
Li Zhang
1,
Xilang Yang
1,
Guijin Shen
1,
Shuo Wang
1,
Haolin Teng
1,
Chunbo Yang
1,
Xueyan Liu
1,
Xiangjing Wang
1,2,
Junwei Zhao
1,* and
Wensheng Xiang
1,2,*
1
Key Laboratory of Agricultural Microbiology of Heilongjiang Province, Northeast Agricultural University, No. 600 Changjiang Road, Xiangfang District, Harbin 150030, China
2
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100097, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2022, 8(11), 1170; https://doi.org/10.3390/jof8111170
Submission received: 19 September 2022 / Revised: 18 October 2022 / Accepted: 4 November 2022 / Published: 6 November 2022
Browse Figures
Review Reports Versions Notes

Abstract

:
Fusarium spp. are among the most important plant pathogens in the world. A survey on maize leaf blight was carried out in Heilongjiang province from 2019 to 2021. Based on morphological characteristics and a phylogenetic analysis on translation elongation factor (tef1) and second-largest subunit of RNA polymerase II (rpb2) genes, 146 Fusarium isolates were obtained and grouped into 14 Fusarium species, including F. ipomoeae (20.5%), F. compactum (17.1%), F. sporotrichioides (9.59%), F. graminearum (9.59%), F. citri (8.9%), F. asiaticum (6.85%), F. verticillioides (6.85%), F. acuminatum (5.48%), F. glycines (5.48%), F. temperatum (2.74%), F. armeniacum (2.74%), Fusarium sp. (2.05%), F. flagelliforme (1.4%), and F. annulatum (0.68%). The Fusarium incarnatum-equiseti species complex (FIESC, including F. ipomoeae, F. compactum, F. citri, and F. flagelliforme) was the most prevalent, indicating an evolving occurrence of the Fusarium species causing maize leaf blight. The typical symptoms observed on the maize leaves were oval to long strip lesions, with a gray to dark gray or brownish red coloration in the center and a chlorotic area at the edges. Based on the tef1 gene, seven haplotypes of FIESC were identified in Heilongjiang province, suggesting a population expansion. This is the first report of F. ipomoeae, F. compactum, F. flagelliforme, F. citri, F. sporotrichioides, F. graminearum, F. asiaticum, F. acuminatum, F. glycines, F. temperatum, F. armeniacum, Fusarium sp., and F. annulatum causing maize leaf blight in Heilongjiang province, China. The current research is informative for managing disease, exploring the phylogenetic relationship among Fusarium species, and clarifying the diversity of Fusarium species associated with maize leaf blight.

1. Introduction

Fusarium spp. can cause several diseases in maize, such as Fusarium ear rot [1,2,3], Fusarium stalk rot and root rot [2,4], seedling blight [5], and maize leaf blight [6]. Regarding maize leaf blight, Fusarium verticillioides was the first pathogen, reported in 1968 [6], to cause the disease, and the only reported one up to now. However, the pathogenicity and diversity of Fusarium spp. causing maize leaf blight are still unclarified. Maize leaf blight is characterized by symptoms of irregular or spindle lesions, with gray to reddish brown coloration in the lesions’ center surrounded by a chlorotic halo. Sometimes, this disease is misjudged as northern corn leaf spot due to the similar symptoms in the field. Thus, the identification of the pathogens based only on disease symptoms in the field is difficult.
To our knowledge, the genus Fusarium includes more than 300 phylogenetic species [7] and is one of the most important plant pathogens in the world [8]. Most species within the genus can produce a diverse range of mycotoxins, causing varying degrees of acute or chronic toxic effects [1]. Therefore, the accurate identification of these mycotoxin producers is a considerable endeavor [9]. For the identification of fungi and the investigation of molecular ecology, the internal transcribed spacer (ITS) is the most sequenced DNA region [10]. However, the ITS region cannot distinguish the species complex of Fusarium due to its conservation [11]. By contrast, the tef1 gene can be used to discriminate Fusarium species at the species or subspecies level [11,12], and the rpb2 gene is also more informative and frequently employed, so it has been recommended that they are sequenced for Fusarium species identification. However, although the partial beta-tubulin gene has been used to identify several Fusarium species, it was not universally informative within Fusarium [13].
The members of Fusarium incarnatum-equiseti species complex (FIESC) are considered important plant pathogens. FIESC is rarely considered the major pathogen of disease epidemics, but it has been identified as a co-occurring fungal pathogen during an infection [14]. Thirty phylogenetic species within the FIESC (FIESC 1 through FIESC 30) were recognized through Multi-locus Sequence Typing (MLST) [15,16], and the species containing multiple haplotypes are designated by the addition of a lowercase letter to the phylogenetic species designation [9].
Phylogenetic and genetic diversity analyses based on multiple sequences can reveal evolutionary relationships associated with geographical regions [9]. High genetic diversity indicates greater adaptability to changing environmental conditions. In some complex evolutionary scenarios, appropriate and sufficient information may not be obtained from phylogenetic trees [17,18]. By comparison, haplotype networks can be employed to analyze the intraspecific diversity of populations, genetic processes, and the biogeography and history of populations [18,19].
To date, there has been little research on pathogenicity, genetic diversity, and the haplotype groups of pathogenic Fusarium species isolated from symptomatic maize leaves in China. Hence, the purposes of the present study were to: (i) describe the morphological characterization and phylogenetic relationships based on tef1 and rpb2 genes of Fusarium species responsible for maize leaf blight in Heilongjiang province, (ii) evaluate the pathogenicity of different Fusarium species, and (iii) determine the haplotype diversity of FIESC based on tef1 associated with maize leaf blight.

2. Materials and Methods

2.1. Fusarium Isolates Collection

From 2019 to 2021, a total of 132 symptomatic maize leaves were collected from 10 different maize-growing counties or cities in Heilongjiang province. The symptomatic maize leaves were cut with a sterilized scalpel, superficially disinfected with a 2% solution of sodium hypochlorite for 1 min and 75% ethanol for 30 s, rinsed thrice with sterile distilled water, and air-dried on sterile filter papers under aseptic conditions. Pure cultures were obtained by single-spore isolation and maintained on PDA (potato dextrose agar) at 25 °C for 7 days. Fusarium isolates were obtained and preserved on PDA slants at 4 °C and 20% glycerol at −80 °C for temporary storage and long-term storage, respectively.

2.2. Morphological Characterization

All Fusarium isolates were incubated on PDA plate in the dark at 25 °C for 7 days. Colony color and colony texture were observed for each isolate. To determine the size of well-developed macroconidia (n = 30) and the number of septa, these Fusarium isolates were incubated on PDA plates at 25°C for 7 days with light/dark cycle of 8/16 h. The macroconidia were observed under light microscopy (Zeiss Axiolab5 equipped with an Axiocam 208 color industrial digital camera).

2.3. DNA Extraction and Sequence Analysis

Fresh mycelia were harvested from cultures grown on PDA supplemented with streptomycin (50 mg/L) and tetracycline (50 mg/L) for 7 days at 28 °C. The extraction of fungal genomic DNA was performed as Ramdial et al. described [9]. The sequences of the translation elongation factor 1-alpha (tef1) gene, second-largest subunit of RNA polymerase II gene (rpb2), and partial beta-tubulin gene were amplified by the primers EF-1/EF-2, RPB2-5f2/RPB2-7cr, and Bt2a/Bt2b [13,20], respectively. The PCR products were sent to Jilin Comate Bioscience Co. Ltd. for purification and sequencing. Sequences of 146 Fusarium isolates were searched against GenBank and FUSARIOID-ID database (www.fusarium.org, accessed date: 1 September 2022) [21] by Basic Local Alignment Search Tool (BLAST) analysis and then deposited into the NCBI GenBank (Table 1).

2.4. Phylogenetic Relationships among Fusarium Isolates

The rpb2 (794–896 bp), tef1(546–686 bp), and β-tubulin (332–356 bp) gene sequences of Fusarium isolates were also compared to the sequences available in the FUSARIOID-ID database (www.fusarium.org, accessed date: 1 September 2022) to collect related sequences for inclusion in phylogenetic analysis. Multiple sequence alignments were correspondingly inferred in Molecular Evolutionary Genetics Analysis (MEGA) 7 software [22] using the MUSCLE (multiple sequence comparison by log-expectation) program [23] and refined manually if necessary. To generate concatenated datasets, single gene sequences (tef1 and rpb2) were manually combined utilizing BioEdit [24]. Phylogenetic tree based on the concatenated sequences of tef1 and rpb2 genes was built using the maximum likelihood (ML) method in MEGA 7, respectively. ML tree was generated from bootstrapping 1000 replicates. Bootstrap values ≥ 70% were shown in phylogenetic trees. The sequences from the Fusarium spp. type strains, initially identified as closely related to the sequences herein, were finally included by the preliminary BLAST searches.

2.5. Pathogenicity Tests

All Fusarium isolates were used to evaluate their pathogenicity based on the method described by Xu et al. [25]. To fulfill Koch’s postulates, 10 healthy, surface-sterilized, and four to five leaf-stage maize seedlings (var. Demeiya 3) for each Fusarium isolate were inoculated with Fusarium spore suspension (1 × 106 spores/mL). Twenty maize seedlings sprayed with sterile distilled water served as controls. All seedlings sealed with plastic bags were maintained in a greenhouse at 25 °C with 90% relative humidity and a light/dark cycle of 12/12 h.
Disease severity (DS) and disease incidence (DI) were assessed 14 days post-inoculation. DS was measured based on a 0–9 scale described by Rafael et al. [26] and Xu et al. [25]: 0 (no visible symptoms), 1 (0 up to 0.5%), 2 (0.5–1.6%), 3 (1.6–5.0%), 4 (5.0–15%), 5 (15–37%), 6 (37–66%), 7 (66–87%), 8 (87% to 96%), and 9 (96–100%). DI was computed by following formula: DI = [100 × ∑ (n × corresponding DS)]/(N × 9), where n is the number of infected inoculation leaves corresponding to each disease rating, and N is the total number of inoculation leaves. Disease incidence was computed by following formula: disease incidence = number of diseased leaves/total number of inoculated leaves of living maize plants. A least significant difference (LSD) test was used for statistical analysis at a significance level of p < 0.05 with the Statistical Package for Social Sciences (SPSS) software (v. 20.0; SPSS Inc., Wacker Drive, Chicago, IL, USA, Illinois.IBM Corp., 2012. IBM). All re-isolated pathogens from inoculated maize leaves were identified using morphological and molecular methods mentioned above. Each experiment was repeated two times.

2.6. DNA Polymorphism

DNA Sequence Polymorphism software version 6 was used to individually determine the DNA polymorphism relative degree of the tef1 gene sequences [27]. Furthermore, Tajima’s D, Fu and Li’s D, and Fu and Li’s F were used to determine neutrality test statistics. Significant values of these tests indicate the presence of population changes [28,29]. DNA polymorphism analyses were only performed on FIESC and not on other Fusarium species on account of the limited number of isolates from those species obtained in the current study.

2.7. Haplotype Analysis

Haplotype networks were individually generated based on the tef1 gene sequences of 70 FIESC isolates (including 30 F. ipomoeae isolates, 25 F. compactum isolates, 13 F. citri isolates, and 2 F. flagelliforme isolates in the present study) using PopART v. 1.7 (Allan Wilson Centre Imaging Evolution Initiative) to evaluate genealogy pattens of the haplotypes [19]. The aligned haplotype sequences were used to construct a TCS network [30,31].

3. Results

3.1. Fungal Isolation and Morphological Characterization

In this study, 146 Fusarium isolates were obtained from symptomatic maize leaves in China (Table 1), which were initially classified into 11 groups based on their morphological features, including the Fusarium incarnatum-equiseti species complex (FIESC, including F. ipomoeae, F. compactum, F. citri, and F. flagelliforme in this study), F. sporotrichioides, F. armeniacum, F. asiaticum, F. graminearum, Fusarium sp., F. acuminatum, F. glycines, F. annulatum, F. temperatum, and F. verticillioides (Table 2).
Seventy isolates were identified as the members of FIESC and produced white to light yellow aerial mycelia. The bottom of the plate turned white to pale brown with time. The macroconidia were slightly curved at the apex with three to five septa and ranged from 39.6 to 83.5 × 3.9 to 5.2 μm (n = 30, Figure 1a–d and Figure 2a–d) in size.
Fourteen F. sporotrichioides isolates produced dense, pinkish white to carmine red aerial mycelia, whose macroconidia were moderately curved to straight with three to five septa, but mostly three-septate, and measured 20.5 to 47.3µm × 2.8 to 4.2 µm (n = 30, Figure 1n and Figure 2f).
The colonies of four F. armeniacum isolates were white to light pink. The macroconidia were prominently curved with three to five septa and had sizes ranging from 35.6 to 59.3 μm × 4 to 4.6 μm (n = 30, Figure 1g and Figure 2g).
Ten isolates producing pink to fluffy dark red aerial mycelia, and red to aubergine pigmentation with age, were classified under F. asiaticum. Their macroconidia were falcate with three to five septa and measured 25.2 to 61.5 × 3.9 to 4.7 μm (n = 30, Figure 1h and Figure 2h).
Fourteen F. graminearum isolates produced white-pink aerial mycelia and had dark red pigmentation. Their macroconidia were straight or slightly curved with five to seven septa and measured 25.4 to 97.7 × 3.4 to 5.8 µm (n = 30, Figure 1k and Figure 2i).
Three Fusarium sp. isolates produced white to yellow colonies and red pigmentation. Their macroconidia were curved with three to five septa and measured 34.0 to 71.6 × 3.2 to 4.7 μm (n = 30, Figure 1j and Figure 2j).
The colonies of eight F. acuminatum isolates were whitish-pink or carmine to rose red. Their macroconidia were slender with a distinct curve of the apical cell, mostly three- to five-septate, and measured 31.3 to 65.3 × 4.0 to 6.5 µm (n = 30, Figure 1f and Figure 2k).
The colonies of eight F. glycines isolates produced fluffy, white aerial hyphae and a dark red pigment. Their macroconidia were three- to seven-septate, slightly curved, and ranged from 53.3 to 117.9 μm × 3.3 to 4.5 μm (n = 30, Figure 1l and Figure 2l) in size.
The aerial mycelia of the F. annulatum isolates were white to cream-colored and turned violet with age, and their macroconidia were straight or slightly curved and contained three to five septa, with sizes of 21.5 to 58.3 × 2.1 to 3.6 µm (n = 30, Figure 1i and Figure 2m).
The colonies of four F. temperatum isolates were pinkish-white and produced mostly three-septate macroconidia. Their macroconidia measured 34.5 to 60.8 × 3.2 to 4.1 µm (n = 30, Figure 1e and Figure 2n).
Ten F. verticillioides isolates formed cottony white to greyish-purple colonies with a dark yellow to purple-gray underside. Their microconidia were abundant and mainly showed clavate shapes measuring 4.2 to 7.5 × 2.1 to 3.8 μm (n = 30, Figure 1m and Figure 2e). However, there were no macroconidia of the F. verticillioides isolates observed in this study.

3.2. Phylogenetic Analysis

The sequences of the tef1, rpb2, and beta-tubulin genes of all the Fusarium isolates obtained in this study were searched against the FUSARIOID-ID database (www.fusarium.org, accessed date: 1 September 2022) using a BLAST analysis (Table S1). For further molecular verification, a multilocus phylogenetic analysis (MLSA) was further performed based on the concatenated sequences (tef1 and rpb2 genes) of all the Fusarium isolates (Figure 3). These results indicated that all the Fusarium isolates could be grouped into 14 clades, including F. ipomoeae, F. compactum, F. sporotrichioides, F. citri, F. graminearum, F. asiaticum, F. verticillioides, F. acuminatum, F.glycines, F. temperatum, F. armeniacum, Fusarium sp., F. flagelliforme, and F. annulatum.

3.3. Pathogenicity Tests

Two weeks after inoculation, the pathogenicity test revealed that all the Fusarium species could cause similar maize leaf blight symptoms (Figure 4). Small oval to fusiform or long striped spots initially appeared on the maize leaves three days post-inoculation, in which the lesions’ centers were gray to reddish brown and surrounded by a chlorotic area. The lesions gradually enlarged with time and merged into each other. In a severe case, the infected leaves were withered. The symptoms observed under greenhouse conditions were similar to the symptoms of maize leaf blight in the field (Figure 4a). No symptoms were observed in the control group. In addition, all the Fusarium species were consistently re-isolated and confirmed based on morphological and molecular methods, while no Fusarium isolates were obtained from the control group, thus fulfilling Koch’s postulates. The average disease incidence and average disease index caused by the Fusarium species ranged from 23 to 74% and from 52 to 85, respectively (Figure 5 and Figure 6; Table S2). Moreover, all the Fusarium isolates were pathogenic towards maize leaves (var. Demeiya 3) and caused maize leaf blight in the inoculation study. In addition, F. graminearum showed the highest virulence, followed by Fusarium sp., F. glycines, F. acuminatum, F. compactum, F. temperatum, F. asiaticum, F. citri, F. verticillioides, F. armeniacum, F. ipomoeae, F. annulatum, F. sporotrichioides, and F. flagelliforme.

3.4. Haplotype Analyses and DNA Polymorphism

The haplotype networks based on the tef1 gene sequences of 70 FIESC isolates (including 30 F. ipomoeae isolates, 25 F. compactum isolates, 2 F. flagelliforme isolates, and 13 F. citri isolates) obtained in this study were used to determine evolutionary relationships among the haplotypes. Most haplotypes within one species were closely related and separated by one to three mutations.
A total of seven haplotypes were identified: the F. ipomoeae isolates were assigned to Hap 1 and 4; F. compactum isolates were assigned to Hap 2, 5, and 6; F. flagelliforme isolates were assigned to Hap 3; and F. citri isolates were assigned to Hap 7 (Figure 7).
Meanwhile, Hap 1, 2, 4, 5, and 7 were shared haplotypes (Figure 7). Hap 1 was the most predominant haplotype, and presented in six locations (Harbin city, Wuchang city, Daqing city, Suihua city, Jixi city, and Qiqihar city). Hap 2 was found in Harbin city and Jixi city. Hap 4 was found in Harbin city and Wuchang city. Hap 5 was distributed in Harbin city and Shuangyashan city. Hap 7 was detected in Harbin city and Qitaihe city. Furthermore, two private haplotypes (Hap 3 and 6) were present in Harbin city and Jixi city, respectively. However, there was no obvious center between these predominant haplotypes. In addition, A low degree of nucleotide diversity (0.02706) and a high degree of haplotype diversity (Hd) (0.778) were found. Tajima’s D, Fu and Li’s D, and Fu and Li’s F tests were negative with no significance (p > 0.10, Table S3).

4. Discussion

As far as we know, this is the first systematic study of the Fusarium species associated with maize leaf blight. In this study, 146 Fusarium isolates delimited to 14 Fusarium species were obtained from symptomatic maize leaves in Heilongjiang province. To analyze the genetic relationship between these Fusarium isolates obtained in the current study, phylogenetic trees were constructed only based on the concatenated sequences of tef1 and rpb2 genes because these two genes were more informative and frequently employed, while the beta-tubulin gene was not universally informative in Fusarium [13]. A total of 14 Fusarium species were identified, including F. ipomoeae, F. compactum, F. sporotrichioides, F. citri, F. graminearum, F. asiaticum, F. verticillioides, F. acuminatum, F. glycines, F. temperatum, F. armeniacum, Fusarium sp., F. flagelliforme, and F. annulatum. Except for F. verticillioides, which was the only reported pathogen inciting maize leaf blight [6], the remaining Fusarium species were all first reported in Heilongjiang province, China, suggesting that the composition of Fusarium species causing maize leaf blight may have changed.
Furthermore, considerable pathogenicity differences were found among the different Fusarium species. F. graminearum showed significantly greater average disease incidence and average disease indices than those of other Fusarium species, followed by Fusarium sp., F. glycines, F. acuminatum, F. compactum, F. temperatum, F. asiaticum, F. citri, F. verticillioides, F. armeniacum, F. ipomoeae, F. annulatum, F. sporotrichioides, and F. flagelliforme. Members of FIESC are generally considered co-occurring pathogens [32,33], and the moderate aggressiveness of FIESC in this study seems to confirm the previous conclusion. FIESC was the most predominant in this study. Members of FIESC have been frequently isolated from maize, soybean, rice, barley, wheat, and so on [34,35,36,37,38,39] and have also been reported to cause leaf blight in peanut plants [40] and Cyperus iria [41].
The haplotype groups of FIESC associated with maize leaf blight were first identified in this work. The predominant haplotype (Hap 1) represented multiple locations (Harbin city, Wuchang city, Daqing city, Suihua city, Jixi city, and Qiqihar city). It is well-known that older haplotypes may have a wider geographic distribution, which suggests that Hap 1 has lasted in the population for a long time [42]. The rest of the haplotypes may represent recently evolved lineages [4]. Furthermore, haplotypes 2, 5, and 6 belonged to the F. compactum clade; haplotypes 1 and 4 belonged to the F. ipomoeae clade; haplotype 3 belonged to the F. flagelliforme clade; and haplotype 7 belonged to the F. citri clade. These FIESC isolates were distributed in different clades in the haplotype network, which suggests that the haplotype network could effectively differentiate the Fusarium species complex and further confirmed our identification results. Moreover, the F. flagelliforme haplotype (Hap 3) and F. citri haplotype (Hap 7) were observed in external parts of the haplotype network and showed more mutation events from their nearest haplotypes, which indicated that these two species have an older evolutionary relationship. In addition, the high haplotype diversity and low nucleotide diversity indicated a population expansion [43].
In conclusion, the current study focused on the pathogenicity and genetic diversity of Fusarium species causing maize leaf blight in Heilongjiang province, China, and is the first to report F. ipomoeae, F. compactum, F. flagelliforme, F. citri, F. sporotrichioides, F. graminearum, F. asiaticum, F. verticillioides, F. acuminatum, F. glycines, F. temperatum, F. armeniacum, Fusarium sp., and F. annulatum as the causal agents. Fusarium can cause various maize diseases; therefore, clarifying the population composition of Fusarium spp. on maize leaves will provide information for the overall control of maize diseases.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof8111170/s1, Table S1. Tef1 gene sequences similarity to reference strain; Table S2. Disease index and disease incidence on maize leaves inoculated with different Fusarium isolates; Table S3. DNA polymorphism data for FIESC isolates based on tef1 gene sequences.

Author Contributions

X.X., L.Z., X.Y., G.S. and S.W. performed the experiments. H.T. and C.Y. prepared the figures and tables. X.X. and X.L. analyzed the data. X.W., W.X. and J.Z. designed the experiments and reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported in part by grants from the Key Program of the National Natural Science Foundation of China (No. 32030090), the Outstanding Youth Project of Natural Science Foundation of Heilongjiang Province (YQ2021C012), the Postdoctoral research fund of Heilongjiang Province (LBH-Q21072), the Academic Backbone Project of Northeast Agricultural University (20XG33), and the National Natural Youth Science Foundation of China (No. 31701858).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Sequences have been deposited in GenBank. The data presented in this study are openly available in NCBI. Publicly available datasets were analyzed in this study. These data can be found here: https://www.ncbi.nlm.nih.gov/, accessed on 3 September 2022.

Conflicts of Interest

The authors declare that there are no conflict of interest.

References

  1. Munkvold, G.P. Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Eur. J. Plant Pathol. 2003, 109, 705–713. [Google Scholar] [CrossRef]
  2. Leslie, J.; Summerell, B.A. The Fusarium Laboratory Manual; Blackwell Publishing: Oxford, UK, 2006. [Google Scholar]
  3. Machado, F.J.; de Barros, A.V.; McMaster, N.; Schmale, D.G., 3rd; Vaillancourt, L.J.; Del Ponte, E.M. Aggressiveness and mycotoxin production by Fusarium meridionale compared with F. graminearum on maize ears and stalks in the field. Phytopathology 2022, 112, 271–277. [Google Scholar] [CrossRef] [PubMed]
  4. Gai, X.T.; Yang, R.X.; Pan, X.J.; Yuan, Y.; Wang, S.N.; Liang, B.B.; Gao, Z.G. First report of Fusarium incarnatum causing stalk rot on maize in China. Plant Dis. 2016, 100, 1010. [Google Scholar] [CrossRef]
  5. Dong, H.; Qin, P.; Gao, Z.; Xu, J.; Xu, X. First report of seedling blight of maize caused by Fusarium asiaticum in Northeast China. Plant Dis. 2021, 105, 1206. [Google Scholar] [CrossRef]
  6. Schieber, R. A leaf blight of corn (Zea mays) incited by Fusarium moniliforme. Phytopathology 1968, 58, 554. [Google Scholar]
  7. Jacobs-Venter, A.; Laraba, I.; Geiser, D.M.; Busman, M.; Vaughan, M.M.; Proctor, R.H.; McCormick, S.P.; O’Donnell, K. Molecular systematics of two sister clades, the Fusarium concolor and F. babinda species complexes, and the discovery of a novel microcycle macroconidium-producing species from South Africa. Mycologia 2018, 110, 1189–1204. [Google Scholar] [CrossRef]
  8. Dean, R.; van Kan, J.A.; Pretorius, Z.A.; Hammond-Kosack, K.E.; Di Pietro, A.; Spanu, P.D.; Rudd, J.J.; Dickman, M.; Kahmann, R.; Ellis, J.; et al. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 2012, 13, 414–430. [Google Scholar] [CrossRef] [Green Version]
  9. Ramdial, H.; Latchoo, R.K.; Hosein, F.N.; Rampersad, S.N. Phylogeny and haplotype analysis of fungi within the Fusarium incarnatum-equiseti species complex. Phytopathology 2017, 107, 109–120. [Google Scholar] [CrossRef] [Green Version]
  10. White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Academic Press: London, UK, 1990; pp. 315–322. [Google Scholar]
  11. O’Donnell, K.; Ward, T.J.; Robert, V.; Crous, P.W.; Geiser, D.M.; Kang, S. DNA sequence-based identification of Fusarium: Current status and future directions. Phytoparasitica 2015, 43, 583–595. [Google Scholar] [CrossRef] [Green Version]
  12. Geiser, D.M.; Jiménez-Gasco, M.D.M.; Kang, S.; Makalowska, I.; Veeraraghavan, N.; Ward, T.J.; Zhang, N.; Kuldau, G.A.; O’Donnell, K. Fusarium-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur. J. Plant Pathol. 2004, 110, 473–479. [Google Scholar] [CrossRef]
  13. O’Donnell, K.; Whitaker, B.K.; Laraba, I.; Proctor, R.H.; Brown, D.W.; Broders, K.; Kim, H.S.; McCormick, S.P.; Busman, M.; Aoki, T.; et al. DNA Sequence-Based Identification of Fusarium: A Work in Progress. Plant Dis. 2022, 106, 1597–1609. [Google Scholar] [CrossRef]
  14. Villani, A.; Moretti, A.; Saeger, S.D.; Han, Z.; Mavungu, J.; Soares, C.; Proctor, R.; Venâncio, A.; Limac, N.; Gaetano, S.; et al. A polyphasic approach for characterization of a collection of cereal isolates of the Fusarium incarnatum-equiseti species complex. Int. J. Food Microbiol. 2016, 234, 24–35. [Google Scholar] [CrossRef] [Green Version]
  15. O’Donnell, K.; Sutton, D.A.; Rinaldi, M.G.; Gueidan, C.; Crous, P.W.; Geiser, D.M. Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-equiseti and F. chalmydosporum species complexes within the United States. J. Clin. Microbiol. 2009, 47, 3851–3861. [Google Scholar] [CrossRef] [Green Version]
  16. O’Donnell, K.; Humber, R.A.; Geiser, D.M.; Kang, S.; Park, B.; Robert, V.A.R.G.; Crous, P.W.; Johnston, P.R.; Aoki, T.; Rooney, A.P.; et al. Phylogenetic diversity of insecticolous Fusariam inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia 2012, 104, 427–445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Huson, D.H.; Bryant, D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23, 254–267. [Google Scholar] [CrossRef] [PubMed]
  18. Blagojević, J.; Vukojevi, J.; Ivanovi, B.; Ivanovi, A. Characterization of Alternaria species associated with leaf spot disease of Armoracia rusticana in Serbia. Plant Dis. 2010, 104, 1378–1389. [Google Scholar] [CrossRef]
  19. Leigh, J.W.; Bryant, D. PopART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 2015, 6, 1110–1116. [Google Scholar] [CrossRef]
  20. Glass, N.L.; Donaldson, G.C. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 1995, 61, 1323–1330. [Google Scholar] [CrossRef] [Green Version]
  21. Crous, P.; Lombard, L.; Sandoval-Denis, M.; Seifert, K.; Schroers, H.-J.; Chaverri, P.; Gené, J.; Guarro, J.; Hirooka, Y.; Bensch, K.; et al. Fusarium: More than a node or a foot-shaped basal cell. Stud. Mycol. 2021, 98, 100116. [Google Scholar] [CrossRef]
  22. Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
  23. Edgar, R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [PubMed]
  24. Raza, M.; Zhang, Z.-F.; Hyde, K.D.; Diao, Y.-Z.; Cai, L. Culturable plant pathogenic fungi associated with sugarcane in southern China. Fungal Divers. 2019, 99, 1–104. [Google Scholar] [CrossRef]
  25. Xu, X.; Zhang, L.; Yang, X.; Cao, H.; Li, J.; Cao, P.; Guo, L.; Wang, X.; Zhao, J.; Xiang, W. Alternaria spp. associated with leaf blight of maize in Heilongjiang Province, China. Plant Dis. 2022, 106, 572–584. [Google Scholar] [CrossRef] [PubMed]
  26. Vieira, R.A.; Mesquini, R.M.; Silva, C.N.; Hata, F.T.; Tessmann, D.J.; Scapim, C.A. A new diagrammatic scale for the assessment of northern corn leaf blight. Crop Prot. 2014, 56, 55–57. [Google Scholar] [CrossRef]
  27. Rozas, J.; Ferrer-Mata, A.; Sánchez-DelBarrio, J.C.; Guirao-Rico, S.; Librado, P.; Ramos-Onsins, S.E.; Sánchez-Gracia, A. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol. Biol. Evol. 2017, 34, 3299–3302. [Google Scholar] [CrossRef]
  28. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123, 585–595. [Google Scholar] [CrossRef]
  29. Fu, Y.X.; Li, W.H. Statistical tests of neutrality of mutations. Genetics 1993, 133, 693–709. [Google Scholar] [CrossRef]
  30. Templeton, A.R.; Crandall, K.A.; Sing, C.F. A cladistics analysis of phenotypic associations with haplotypes inferred from restriction endo nuclease mapping and DNA sequence data III. Cladogram estimation. Genetics 1992, 132, 619–633. [Google Scholar] [CrossRef]
  31. Clement, M.; Snell, Q.; Walke, P.; Posada, D.; Crandall, K.A. TCS: Estimating gene genealogies. In Proceedings of the 16th International Parallel and Distributed Processing Symposium (IPDPS 2002), Fort Lauderdale, FL, USA, 15–19 April 2002. [Google Scholar]
  32. Summerell, B.A.; Salleh, B.; Leslie, J.F. A utilitarian approach to Fusarium identification. Plant Dis. 2003, 87, 117–128. [Google Scholar] [CrossRef] [Green Version]
  33. Jurado, M.; Vázquez, C.; Patiño, B.; González-Jaén, M.T. PCR detection assays for the trichothecene-producing species Fusarium graminearum, Fusarium culmorum, Fusarium poae, Fusarium equiseti and Fusarium sporotrichioides. Syst. Appl. Microbiol. 2005, 28, 562–568. [Google Scholar] [CrossRef]
  34. Wang, M.M.; Chen, Q.; Diao, Y.Z.; Duan, W.J.; Cai, L. Fusarium incarnatum-equiseti complex from China. Pers. Mol. Phylogeny Evol. Fungi 2019, 43, 70–89. [Google Scholar] [CrossRef] [PubMed]
  35. Marín, P.; Moretti, A.; Ritieni, A.; Jurado, M.; Vázquez, C.; González-Jaén, M.T. Phylogenetic analyses and toxigenic profiles of Fusarium equiseti and Fusarium acuminatum isolated from cereals from southern Europe. Food Microbiol. 2012, 31, 229–237. [Google Scholar] [CrossRef] [Green Version]
  36. Barros, G.; Zanon, M.S.; Palazzini, J.M.; Haidukowski, M.; Pascale, M.; Chulze, S. Trichothecenes and zearalenone production by Fusarium equiseti and Fusarium semitectum species isolated from Argentinean soybean. Food Addit. Contam.-Chem. Anal. Control Expo. Risk Assess. 2012, 29, 1436–1442. [Google Scholar] [CrossRef] [PubMed]
  37. Avila, C.F.; Moreira, G.M.; Nicolli, C.P.; Gomes, L.B.; Abreu, L.M.; Pfenning, L.H.; Haidukowski, M.; Moretti, A.; Logrieco, A.; Del Ponte, E.M. Fusarium incarnatum-equiseti species complex associated with Brazilian rice: Phylogeny, morphology and toxigenic potential. Int. J. Food Microbiol. 2019, 306, 108267. [Google Scholar] [CrossRef] [PubMed]
  38. Piacentini, K.C.; Rocha, L.O.; Savi, G.D.; Carnielli-Queiroz, L.; De Carvalho Fontes, L.; Correa, B. Assessment of toxigenic Fusarium species and their mycotoxins in brewing barley grains. Toxins 2019, 11, 31. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Castellá, G.; Cabañes, F.J. Phylogenetic diversity of Fusarium incarnatum-equiseti species complex isolated from Spanish wheat. Antonie Van Leeuwenhoek 2014, 106, 309–317. [Google Scholar] [CrossRef]
  40. Thirumalaisamy, P.P.; Dutta, R.; Jadon, K.S.; Nataraja, M.V.; Padvi, R.D.; Rajyaguru, R.; Yusufzai, S. Association and characterization of the Fusarium incarnatum-F. equiseti species complex with leaf blight and wilt of peanut in India. J. Gen. Plant Pathol. 2018, 85, 83–89. [Google Scholar] [CrossRef]
  41. Gupta, V.S.; Razdan, V.K.; John, D.T.; Sharma, B.C. First report of leaf blight of Cyperus iria caused by Fusarium equiseti in India. Plant Dis. 2013, 97, 838. [Google Scholar] [CrossRef]
  42. Posada, D.; Crandall, K.A. Evaluation of methods for detecting recombination from DNA sequences: Computer simulations. Proc. Natl. Acad. Sci. USA 2001, 98, 13757–13762. [Google Scholar] [CrossRef] [Green Version]
  43. Matić, S.; Tabone, G.; Garibaldi, A.; Gullino, M.L. Alternaria leaf spot caused by Alternaria species: An emerging problem on ornamental plants in Italy. Plant Dis. 2020, 104, 2275–2287. [Google Scholar] [CrossRef]
Jof 08 01170 g001 550
Figure 1. Macroconidia or microconidia of representative isolates of 14 Fusarium species. (a) F. compactum; (b) F. ipomoeae; (c) F. citri; (d) F. flagelliforme; (e) F. temperatum; (f) F. acuminatum; (g) F. armeniacum; (h) F. asiaticum; (i) F. annulatum; (j) Fusarium sp.; (k); F. graminearum; (l) F. glycines; (m) F. verticillioides; (n) F. sporotrichioides.
Figure 1. Macroconidia or microconidia of representative isolates of 14 Fusarium species. (a) F. compactum; (b) F. ipomoeae; (c) F. citri; (d) F. flagelliforme; (e) F. temperatum; (f) F. acuminatum; (g) F. armeniacum; (h) F. asiaticum; (i) F. annulatum; (j) Fusarium sp.; (k); F. graminearum; (l) F. glycines; (m) F. verticillioides; (n) F. sporotrichioides.
Jof 08 01170 g001
Jof 08 01170 g002 550
Figure 2. Colony appearance of representative isolates of 14 Fusarium species. (a) F. compactum; (b) F. ipomoeae; (c) F. citri; (d) F. flagelliforme; (e) F. verticillioides (f) F. sporotrichioides; (g) F. armeniacum; (h) F. asiaticum; (i) F. graminearum; (j) Fusarium sp.; (k) F. acuminatum; (l) F. glycines; (m) F. annulatum; (n) F. temperatum.
Figure 2. Colony appearance of representative isolates of 14 Fusarium species. (a) F. compactum; (b) F. ipomoeae; (c) F. citri; (d) F. flagelliforme; (e) F. verticillioides (f) F. sporotrichioides; (g) F. armeniacum; (h) F. asiaticum; (i) F. graminearum; (j) Fusarium sp.; (k) F. acuminatum; (l) F. glycines; (m) F. annulatum; (n) F. temperatum.
Jof 08 01170 g002
Jof 08 01170 g003 550
Figure 3. Phylogenetic tree obtained from maximum likelihood analysis based on the concatenated sequences of tef1 and rpb2 genes. Support values at nodes representing RA × ML bootstrap percentages with values ≥70 are shown above the branches.
Figure 3. Phylogenetic tree obtained from maximum likelihood analysis based on the concatenated sequences of tef1 and rpb2 genes. Support values at nodes representing RA × ML bootstrap percentages with values ≥70 are shown above the branches.
Jof 08 01170 g003
Jof 08 01170 g004 550
Figure 4. (a) Leaf blight symptoms on maize leaves caused by Fusarium species in the field; (b–o) Typical symptoms observed in greenhouse on maize leaves after inoculation with: (b) F. ipomoeae; (c) F. compactum; (d) F. flagelliforme; (e) F. asiaticum; (f) F. armeniacum; (g) F. citri; (h) F. sporotrichioides; (i) Fusarium sp.; (j) F. glycines; (k) F. graminearum; (l) F. annulatum; (m) F. temperatum; (n) F. verticillioides; (o) F. acuminatum.
Figure 4. (a) Leaf blight symptoms on maize leaves caused by Fusarium species in the field; (b–o) Typical symptoms observed in greenhouse on maize leaves after inoculation with: (b) F. ipomoeae; (c) F. compactum; (d) F. flagelliforme; (e) F. asiaticum; (f) F. armeniacum; (g) F. citri; (h) F. sporotrichioides; (i) Fusarium sp.; (j) F. glycines; (k) F. graminearum; (l) F. annulatum; (m) F. temperatum; (n) F. verticillioides; (o) F. acuminatum.
Jof 08 01170 g004
Jof 08 01170 g005 550
Figure 5. Disease index for maize leaves inoculated with different Fusarium species.
Figure 5. Disease index for maize leaves inoculated with different Fusarium species.
Jof 08 01170 g005
Jof 08 01170 g006 550
Figure 6. Disease incidence for maize leaves inoculated with different Fusarium species. Outliers are represented by a hollow circle.
Figure 6. Disease incidence for maize leaves inoculated with different Fusarium species. Outliers are represented by a hollow circle.
Jof 08 01170 g006
Jof 08 01170 g007 550
Figure 7. TCS analyses and the haplotype distribution based on the tef1 gene sequences of 70 FIESC isolates obtained in this study. Each haplotype is represented by a circle, the size of which is proportional to the haplotype frequency.
Figure 7. TCS analyses and the haplotype distribution based on the tef1 gene sequences of 70 FIESC isolates obtained in this study. Each haplotype is represented by a circle, the size of which is proportional to the haplotype frequency.
Jof 08 01170 g007
Table
Table 1. List of GenBank accession numbers of Fusarium isolates obtained from symptomatic maize leaves collected from Heilongjiang province and reference strains used in this study.
Table 1. List of GenBank accession numbers of Fusarium isolates obtained from symptomatic maize leaves collected from Heilongjiang province and reference strains used in this study.
Isolates.Latitude and LongitudeSpeciesGenBank Accession Nos.
tef1rpb2Beta-Tubulin
HA-z142126.738196, 45.753014F. ipomoeaeOM985077OP436018OP642121
HA-z11126.738196, 45.753014F. ipomoeaeOM985078OP436019OP642120
HA-z12126.738196, 45.753014F. ipomoeaeOM985079OP436020OP642119
HA-z13126.738196, 45.753014F. ipomoeaeOM985080OP436021OP642118
HA-z14126.738196, 45.753014F. ipomoeaeOM985081OP436022OP642117
HA-z15126.738196, 45.753014F. ipomoeaeOM985082OP436023OP642116
HA-z16126.738196, 45.753014F. ipomoeaeOM985083OP436024OP642115
HA-z17126.738196, 45.753014F. ipomoeaeOM985084OP436025OP642114
HA-z18126.738196, 45.753014F. ipomoeaeOM985085OP436026OP642113
HA-z19126.738196, 45.753014F. ipomoeaeOM985086OP436027OP642112
HA-z20126.738196, 45.753014F. ipomoeaeOM985087OP436028OP642111
HA-z21126.738196, 45.753014F. ipomoeaeOM985088OP436029OP642110
HA-z22126.738196, 45.753014F. ipomoeaeOM985089OP436030OP642109
HA-x22126.868024, 45.850128F. ipomoeaeOM985106OP436031OP642108
HA-xy82126.933932, 45.769353F. ipomoeaeOM985109OP436032OP642122
HA-xy83126.933932, 45.769353F. ipomoeaeOM985110OP436033OP642123
HA-31126.868024, 45.850128F. ipomoeaeOM985118OP436034OP642107
SH-11127.270457, 46.64457F. ipomoeaeOM985119OP436035OP642106
SH-63127.270457, 46.64457F. ipomoeaeOM985120OP436036OP642105
WC-31127.22506, 44.93996F. ipomoeaeOM985124OP436037OP642104
QQ-41124.340195, 47.29158F. ipomoeaeOM985125OP436038OP642103
SH-62127.270457, 46.64457F. ipomoeaeOM985126OP436039OP642124
HA-z201126.738196, 45.753014F. ipomoeaeOM985127OP436040OP642125
HA-21126.868024, 45.850128F. ipomoeaeOM985128OP436041OP642126
HA-22126.868024, 45.850128F. ipomoeaeOM985129OP436042OP642127
HA-x21126.868024, 45.850128F. ipomoeaeOM985130OP436043OP642102
HA-212126.868024, 45.850128F. ipomoeaeOM985140OP436044OP642101
DQ-n22125.835845, 46.329205F. ipomoeaeOM985182OP436045OP642100
JX-21132.477436, 46.339951F. ipomoeaeOM985183OP436046OP642098
DQ-n31125.835845, 46.329205F. ipomoeaeOM985184OP436047OP642099
HA-61126.868024, 45.850128F. compactumOM985144OP435951OP642130
HA-111126.868024, 45.850128F. compactumOM985102OP435952OP642131
JX-y11132.477436, 46.339951F. compactumOM985123OP435953OP642132
HA-621126.868024, 45.850128F. compactumOM985145OP435975OP642128
SYS-31132.768479, 46.215238F. compactumOM985146OP435954OP642129
HA-z152126.738196, 45.753014F. compactumOM985147OP435955OP642133
HA-z31126.738196, 45.753014F. compactumOM985148OP435956OP642134
HA-z32126.738196, 45.753014F. compactumOM985149OP435957OP642135
HA-z33126.738196, 45.753014F. compactumOM985150OP435958OP642136
HA-z34126.738196, 45.753014F. compactumOM985151OP435959OP642137
HA-z35126.738196, 45.753014F. compactumOM985152OP435960OP642138
HA-z36126.738196, 45.753014F. compactumOM985153OP435961OP642139
HA-z37126.738196, 45.753014F. compactumOM985154OP435962OP642140
HA-z38126.738196, 45.753014F. compactumOM985155OP435963OP642141
HA-z39126.738196, 45.753014F. compactumOM985156OP435964OP642142
HA-z310126.738196, 45.753014F. compactumOM985157OP435965OP642143
HA-z311126.738196, 45.753014F. compactumOM985158OP435966OP642144
HA-z312126.738196, 45.753014F. compactumOM985159OP435967OP642145
HA-xy151126.933932, 45.769353F. compactumOM985160OP435968OP642146
HA-xy31126.933932, 45.769353F. compactumOM985161OP435969OP642147
HA-a11126.868024, 45.850128F. compactumOM985162OP435970OP642152
HA-42126.868024, 45.850128F. compactumOM985163OP435971OP642148
JX-52132.477436, 46.339951F. compactumOM985164OP435972OP642149
JX-121132.477436, 46.339951F. compactumOM985165OP435973OP642150
JX-31132.477436, 46.339951F. compactumOM985166OP435974OP642151
HA-x12126.868024, 45.850128F. citriOM985167OP435950OP642166
QTH-21131.139405, 45.733699F. citriOM985168OP435949OP642167
HA-z1125126.738196, 45.753014F. citriOM985169OP435948OP642158
HA-z171126.738196, 45.753014F. citriOM985170OP435947OP642165
HA-z172126.738196, 45.753014F. citriOM985171OP435946OP642164
HA-z173126.738196, 45.753014F. citriOM985172OP435945OP642163
HA-z174126.738196, 45.753014F. citriOM985173OP435944OP642162
HA-z175126.738196, 45.753014F. citriOM985174OP435943OP642161
HA-z176126.738196, 45.753014F. citriOM985175OP435942OP642160
HA-z177126.738196, 45.753014F. citriOM985176OP435941OP642159
HA-z1126126.738196, 45.753014F. citriOM985177OP435940OP642157
HA-xy141126.933932, 45.769353F. citriOM985178OP435939OP642156
HA-z203126.738196, 45.753014F. citriOM985179OP435938OP642155
HA-x11126.868024, 45.850128F. flagelliformeOM985104OP435921OP642153
HA-x51126.868024, 45.850128F. flagelliformeOM985105OP435920OP642154
HA-a31126.868024, 45.850128F. graminearumOM985090OP435980OP642200
HG-11130.440826, 47.312952F. graminearumOM985091OP435981OP642201
QTH-23131.139405, 45.733699F. graminearumOM985103OP435982OP642202
SH-x72127.270457, 46.64457F. graminearumOM985108OP435983OP642203
SYS-y21132.768479, 46.215238F. graminearumOM985111OP435984OP642204
SYS-21132.768479, 46.215238F. graminearumOM985199OP435985OP642205
SYS-141132.768479, 46.215238F. graminearumOM985200OP435986OP642206
SYS-142132.768479, 46.215238F. graminearumOM985201OP435987OP642207
SYS-143132.768479, 46.215238F. graminearumOM985202OP435988OP642208
SYS-144132.768479, 46.215238F. graminearumOM985203OP435989OP642209
SYS-145132.768479, 46.215238F. graminearumOM985204OP435990OP642210
SYS-146132.768479, 46.215238F. graminearumOM985205OP435991OP642211
SYS-147132.768479, 46.215238F. graminearumOM985206OP435992OP642212
HA-a142126.868024, 45.850128F. graminearumOM985138OP435993OP642213
SYS-x71131.583118, 46.462499F. asiaticumOM985092OP436053OP642088
SYS-x91131.583118, 46.462499F. asiaticumOM985093OP436054OP642089
HA-x72126.868024, 45.850128F. asiaticumOM985094OP436055OP642090
HG-x62130.440826, 47.312952F. asiaticumOM985095OP436056OP642091
SYS-x62131.583118, 46.462499F. asiaticumOM985096OP436057OP642092
SYS-x131131.583118, 46.462499F. asiaticumOM985097OP436058OP642093
SYS-x132131.583118, 46.462499F. asiaticumOM985098OP436059OP642094
SYS-x133131.583118, 46.462499F. asiaticumOM985099OP436060OP642095
SYS-x134131.583118, 46.462499F. asiaticumOM985100OP436061OP642096
SYS-x135131.583118, 46.462499F. asiaticumOM985101OP436062OP642097
HA-zh142126.738196, 45.753014F. temperatumOM985107OP436049OP642174
QTH-X332131.139405, 45.733699F. temperatumOM985131OP436050OP642171
QTH-X331131.139405, 45.733699F. temperatumOM985132OP436051OP642173
QTH-X33131.139405, 45.733699F. temperatumOM985133OP436052OP642172
HA-z113126.738196, 45.753014Fusarium sp.OM985112OP436063OP642168
HA-b113126.738196, 45.753014Fusarium sp.OM985113OP436064OP642170
HA-Z1131126.738196, 45.753014Fusarium sp.OM985143OP436065OP642169
SYS-x11131.583118, 46.462499F. sporotrichioidesOM985209OP436017OP642176
SYS-x61131.583118, 46.462499F. sporotrichioidesOM985210OP436016OP642177
SYS-x1131.583118, 46.462499F. sporotrichioidesOM985211OP436015OP642178
SYS-x2131.583118, 46.462499F. sporotrichioidesOM985212OP436014OP642179
HG-12130.440826, 47.312952F. sporotrichioidesOM985213OP436013OP642180
SYS-33132.768479, 46.215238F. sporotrichioidesOM985214OP436012OP642181
SYS-101132.768479, 46.215238F. sporotrichioidesOM985215OP436011OP642182
SYS-102132.768479, 46.215238F. sporotrichioidesOM985216OP436010OP642183
SYS-103132.768479, 46.215238F. sporotrichioidesOM985217OP436009OP642184
SYS-104132.768479, 46.215238F. sporotrichioidesOM985218OP436008OP642185
SYS-105132.768479, 46.215238F. sporotrichioidesOM985219OP436007OP642186
SYS-51132.768479, 46.215238F. sporotrichioidesOM985220OP436006OP642187
HG-y102130.440826, 47.312952F. sporotrichioidesOM985121OP436005OP642188
HG-DBy101130.440826, 47.312952F. sporotrichioidesOM985122OP436004OP642189
SH-z61127.270457, 46.64457F. acuminatumOM985115OP435923OP642072
SH-61127.270457, 46.64457F. acuminatumOM985116OP435922OP642073
SH-41127.270457, 46.64457F. acuminatumOM985117OP435924OP642074
HA-a72126.868024, 45.850128F. acuminatumOM985221OP435925OP642075
HA-a161126.868024, 45.850128F. acuminatumOM985222OP435926OP642076
HA-a162126.868024, 45.850128F. acuminatumOM985223OP435927OP642077
HA-a163126.868024, 45.850128F. acuminatumOM985224OP435928OP642078
HA-a164126.868024, 45.850128F. acuminatumOM985225OP435929OP642079
HA-a1211126.868024, 45.850128F. armeniacumOM985134OP435979OP642214
HA-13126.868024, 45.850128F. armeniacumOM985135OP435978OP642215
HA-a121126.868024, 45.850128F. armeniacumOM985136OP435976OP642216
HA-a122126.868024, 45.850128F. armeniacumOM985137OP435977OP642217
HL-42132.943466, 45.768947F. verticillioidesOM985139OP435994OP642190
DQ-n32125.835845, 46.329205F. verticillioidesOM985141OP435995OP642191
SH-n12127.270457, 46.64457F. verticillioidesOM985142OP435996OP642192
JX-123132.477436, 46.339951F. verticillioidesOM985181OP435997OP642193
SH-n11127.270457, 46.64457F. verticillioidesOM985187OP435998OP642194
SH-n201127.270457, 46.64457F. verticillioidesOM985188OP435999OP642195
SH-n202127.270457, 46.64457F. verticillioidesOM985189OP436000OP642197
SH-n203127.270457, 46.64457F. verticillioidesOM985190OP436001OP642197
SH-n204127.270457, 46.64457F. verticillioidesOM985191OP436002OP642199
SH-n205127.270457, 46.64457F. verticillioidesOM985192OP436003OP642199
JX-3352132.477436, 46.339951F. glycinesOM985193OP435937OP642080
JX-335132.477436, 46.339951F. glycinesOM985194OP435930OP642081
HA-171126.868024, 45.850128F. glycinesOM985195OP435936OP642082
HA-172126.868024, 45.850128F. glycinesOM985196OP435935OP642083
HA-173126.868024, 45.850128F. glycinesOM985197OP435934OP642084
HA-174126.868024, 45.850128F. glycinesOM985198OP435933OP642085
WC-b53127.22506, 44.93996F. glycinesOM985208OP435932OP642086
HA-z1412126.738196, 45.753014F. glycinesOM985180OP435931OP642087
WC-22127.22506, 44.93996F. annulatumOM985207OP436048OP642175
NRRL 34034-F. ipomoeaeGQ505636GQ505814-
LC0455-F. ipomoeaeMK289580MK289734-
NRRL 45996-F. ipomoeaeGQ505671GQ505849-
CBS 140909-F. ipomoeaeMN170479MN170412-
NRRL 28029-F. compactumGQ505602GQ505780-
NRRL 36318-F. compactumGQ505646GQ505824-
NRRL 6548-F. flagelliformeGQ505589GQ505767-
CBS 731.87-F. flagelliformeGQ505600GQ505778-
LC12147-F. arcuatisporumMK289584MK289739-
NRRL 32997-F. arcuatisporumGQ505624GQ505802-
NRRL 45997-F. clavusGQ505672GQ505850-
NRRL 34037-F. clavusGQ505638GQ505638-
LC7937-F. citriMK289640GQ505816-
LC7922-F. citriMK289634MK289788-
NRRL 66939-Fusarium sp.MW233217MW233561-
FRC R-9121-Fusarium sp.MW233213MW233557-
CBS 462.94-F. sporotrichioidesMN120771MN120750-
NRRL 53430-F. sibiricumHM744684MW233474-
NRRL 6227-F. armeniacumHM744692JX171560-
FRC R-09335-F. armeniacumGQ915501GQ915485-
NRRL 13818-F. asiaticumAF212451MW233412-
NRRL 46738-F. asiaticumFJ240299--
NL19-100008-F. graminearumMZ921906MZ921775-
CBS 136009-F. graminearumMW928838MW928826-
NRRL 54216-F. acuminatumHM068314HM068334-
JW 289003-F. acuminatumMZ921908MZ921777-
CBS 130180-F. verticillioidesMW402024MW402740-
CBS 131389-F. verticillioidesMN534047MN534288-
CBS 135541-F. temperatumMW402051KU604284-
CBS 130323-Fusarium sp.MH485018MH484927-
CBS 214.49-F. glycinesMH484960MH484869-
CBS 127316-F. annulatumMW402021MW402738-
CBS 100001-Macroconia leptosphaeriaeKM231959HQ728164-
Bold accession numbers were generated from other studies.
Table
Table 2. Geographic origins and number of Fusarium isolates recovered from symptomatic maize leaves with macroscopic symptoms of leaf blight collected from 10 locations in Heilongjiang province, China.
Table 2. Geographic origins and number of Fusarium isolates recovered from symptomatic maize leaves with macroscopic symptoms of leaf blight collected from 10 locations in Heilongjiang province, China.
Geographic OriginsNumber of Fusarium Isolates
FIESCF. sporotrichioidesF. armeniacumF. asiaticumF. graminearumFusarium sp.F. acuminatumF. glycinesF. annulatumF. temperatumF. verticillioides
Daqing city20000000001
Harbin city 560412355010
Hegang city03011000000
Jixi city50000002001
Qiqihar city10000000000
Qitaihe city10001000030
Shuangyashan city111089000000
Suihua city30001030007
Hulin country00000000001
Wuchang city10000001100
Total7014410143881410
Percentage a47.959.592.746.859.592.055.485.480.682.746.85
a Percentage = n/N × 100%, where n is the number of isolates for one species of Fusarium, and N is the total number of isolates for all Fusarium species.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Xu, X.; Zhang, L.; Yang, X.; Shen, G.; Wang, S.; Teng, H.; Yang, C.; Liu, X.; Wang, X.; Zhao, J.; et al. Fusarium Species Associated with Maize Leaf Blight in Heilongjiang Province, China. J. Fungi 2022, 8, 1170. https://doi.org/10.3390/jof8111170

AMA Style

Xu X, Zhang L, Yang X, Shen G, Wang S, Teng H, Yang C, Liu X, Wang X, Zhao J, et al. Fusarium Species Associated with Maize Leaf Blight in Heilongjiang Province, China. Journal of Fungi. 2022; 8(11):1170. https://doi.org/10.3390/jof8111170

Chicago/Turabian Style

Xu, Xi, Li Zhang, Xilang Yang, Guijin Shen, Shuo Wang, Haolin Teng, Chunbo Yang, Xueyan Liu, Xiangjing Wang, Junwei Zhao, and et al. 2022. "Fusarium Species Associated with Maize Leaf Blight in Heilongjiang Province, China" Journal of Fungi 8, no. 11: 1170. https://doi.org/10.3390/jof8111170

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop