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Research Article
Curvularia microspora sp. nov. associated with leaf diseases of Hippeastrum striatum in China
expand article infoYin Liang, Shuang-Fei Ran, Jayarama Bhat§, Kevin D. Hyde|, Yong Wang, De-Gang Zhao
‡ Guizhou University, Guiyang, China
§ Goa University, Goa, India
| Mae Fah Luang University, Chiang Rai, Thailand
¶ Guizhou Academy of Agricultural Sciences, Guiyang, China
Open Access

Abstract

An undescribed Curvularia sp. was isolated from the leaf spot disease of Barbados Lily (Hippeastrum striatum (Lam.) Moore). Phylogenetic analyses of combined ITS, 28S, GPD1 and TEF1 sequence data place nine strains of this species in the trifolii-clade, but they clustered together as an independent lineage with strong support. This species was morphologically compared with related species in the trifolii-clade. Based on differences in morphology and phylogeny, it is concluded that this species is a new taxon, introduced as Curvularia microspora sp. nov. Pathogenicity testing determined the new species to be pathogenic on H. striatum.

Keywords

China, hyphomycetes, identify, pathogen, taxonomy

Introduction

The genus Curvularia includes pathogens and saprobes of various plants, as well as opportunistic pathogens of humans and animals (Sivanesan 1987, Manamgoda et al. 2011, 2012, da Cunha et al. 2013, Hyde et al. 2014) and has been well-studied in recent years. Identification of Curvularia spp. was previously mainly based on morphological descriptions and comparisons, however, the use of molecular taxonomy has solved many problems of resolving species (Valente et al. 1999, Mendoza et al. 2001). A multi-gene phylogenetic tree, based on the internal transcribed spacers including the 5.8S nuclear ribosomal DNA gene (ITS), the 5’ end of the nuclear ribosomal large subunit (28S), fragments of the glycerol-3-phosphate dehydrogenase (GPD1) and translational elongation factor EF-1 alpha (TEF1) gene regions, was provided to identify fresh collections of Curvularia from various hosts and geographic locations worldwide (Manamgoda et al. 2015).

In this study, DNA sequences of ITS, 28S, GPD1 and TEF1 gene regions were used for phylogenetic analyses to identify a new Curvularia species. This was concluded based on the combined morphology and phylogeny. Curvularia microspora sp. nov., is introduced here, associated with leaf diseases of Hippeastrum striatum.

Materials and methods

Isolation and morphological studies

All diseased samples were collected from the Medical Plants Herb Garden, in Chongqing City, Nanchuan County, China. This garden is located in a region of subtropical humid monsoon climate and has conserved more than 3000 kinds of medicinal plants. In this study, all fungal strains were isolated by the single-spore technique in order to obtain pure cultures following the method of Chomnunti et al. (2014). Single spores were transferred to potato-dextrose agar (PDA) and incubated at room temperature (28 °C). After several weeks of incubation, the morphological characters were recorded following the methods of Manamgoda et al. (2011, 2012). Conidia and conidiophores were observed using a compound microscope (Nikon Eclipse E600 DIC microscope and a Nikon DS-U2 camera or a Nikon 80i compound microscope fitted with a Canon 450D digital camera). The holotype specimen was deposited in the Herbarium of the Department of Plant Pathology, Agricultural College, Guizhou University (HGUP). Ex-type cultures were also deposited in the culture collection at the Department of Plant Pathology, Agriculture College, Guizhou University, P.R. China (GUCC).

DNA extraction and sequencing

Fungal cultures were grown on PDA until nearly covering the whole Petri-dish (90 mm) at 28 °C. Fresh fungal mycelia were scraped with sterilised scalpels. A BIOMIGA Fungus Genomic DNA Extraction Kit (GD2416) was used to extract fungal genome DNA. DNA Amplification was performed in a 25 μL reaction volume which contained 2.5 μL 10 × PCR buffer, 1 μL of each primer (10 μM), 1 μL template DNA and 0.25 μL Taq DNA polymerase (Promega, Madison, WI, USA). Primers ITS4 and ITS5 (White et al. 1990) were used to amplify the ITS region. The thermal cycling programme was: 3 min initial denaturation at 95 °C, followed by 30 cycles of 30 s denaturation at 94 °C, 30 s primers annealing at 52 °C, 1 min extension at 72 °C and a total 10 min extension at 72 °C. To amplify the GPD1 gene, the primers gpd1 and gpd2 were used (Berbee et al. 1999). The amplification programme included an initial denaturation step at 96 °C for 2 min, followed by 35 PCR cycles with 1 min at 96 °C, 1 min at 52 °C and 45 s at 72 °C with a final 10 min extension at 72 °C. The TEF1 and 28S regions were amplified using EF-526F/1567R and LR5/LROR primers respectively (Schoch et al. 2009). The 28S amplification programme included an initial denaturation step at 95 °C for 3 min followed by 30 cycles of 40 s denaturation at 94 °C, 50 s primer annealing at 52 °C, 1 min extension at 72 °C. The same PCR reaction was used to amplify TEF1 with the only change being the annealing temperature at 54 °C.

Phylogenetic analysis

DNA sequences from these isolates and reference sequences were downloaded from GenBank and analysed by maximum parsimony (MP) and maximum likelihood (ML) (Table 1). Sequences were optimised manually to allow maximum alignment and maximum sequence similarity, as detailed in Manamgoda et al. (2012). The alignment document of four phylogenetic markers has been submitted to TreeBase (https://treebase.org/; Accession number: 21970). A partition homogeneity test (PHT) was performed with 1000 replicates via PAUP v. 4.0b10 (Swofford 2003) to evaluate statistical congruence amongst sequence data of 28S, ITS, GPD1 and TEF1 gene regions. MP analyses were performed in PAUP v. 4.0b10 (Swofford 2003), using the heuristic search option with 1,000 random taxa addition and tree bisection and reconnection (TBR) as the branch swapping algorithm. Maxtrees were set to 10,000. The characters in the alignment document were ordered accordingly: 28S+ITS+GPD1+TEF1, with equal weight and gaps were treated as missing data. The Tree Length (TL), Consistency Indices (CI), Retention Indices (RI), Rescaled Consistency Indices (RC) and Homoplasy Index (HI) were calculated for each tree generated. Maximum likelihood (ML) trees of DNA sequences were obtained by a heuristic search using the TrN + I + G model, which was deduced as the best fit for the data by the likelihood ratio test using the MODELTEST wer3.7 and MrMTgui version 1.01 (Posada and Crandall 1998).

GenBank accession numbers of isolates include in this study.

Species Isolate GenBank accesssion numbers and references
ITS 28S GPD1 TEF1
Alternaria alternata EGS 34.0160 AF071346 Berbee et al. 1999 AF081400 Berbee et al. 1999
Curvularia akaii CBS 318.86 HF934921 Amaradasa et al. 2014 HG779118 Madrid et al. 2014
C. borreriae CBS 859.73 HE861848 da Cunha et al. 2013 HF565455 da Cunha et al. 2013
C. borreriae MFLUCC 11-0442 KP400638 Manamgoda et al. 2015 KP419987 Manamgoda et al. 2015
C. gladioli ICMP 6160 JX256426 Manamgoda et al. 2012 JX256393 Manamgoda et al. 2012 JX276438 Manamgoda et al. 2012 JX266595 Manamgoda et al. 2012
C. gudauskasii DAOM 165085 AF071338 Berbee et al. 1999 AF081393 Berbee et al. 1999
C. heteropogonis CBS 284.91 JN192379 Manamgoda et al. 2011 JN600990 Manamgoda et al. 2011 JN600969 Manamgoda et al. 2011 JN601013 Manamgoda et al. 2011
C. ovariicola BRIP 15882 JN192384 Manamgoda et al. 2011 JN600992 Manamgoda et al. 2011 JN600971 Manamgoda et al. 2011 JN601020 Manamgoda et al. 2011
C. pallescens CBS 156.35 KJ922380 Manamgoda et al. 2014 KM243269 Manamgoda et al. 2014 KM083606 Manamgoda et al. 2014 KM196570 Manamgoda et al. 2014
C. ravenelii BRIP 13165 JN192386 Manamgoda et al. 2011 JN601001 Manamgoda et al. 2011 JN600978 Manamgoda et al. 2011 JN601024 Manamgoda et al. 2011
C. trifolii AR5169 KP400656 Manamgoda et al. 2015 KP645345 Manamgoda et al. 2015 KP735694 Manamgoda et al. 2015
C. trifolii ICMP 6149 JX256434 Manamgoda et al. 2012 JX256402 Manamgoda et al. 2012 JX276457 Manamgoda et al. 2012 JX266600 Manamgoda et al. 2012
C. tripogonis BRIP 12375 JN192388 Manamgoda et al. 2011 JN601002 Manamgoda et al. 2011 JN600980 Manamgoda et al. 2011 JN601025 Manamgoda et al. 2011
Curvularia sp. ICMP 10344 JX256444 Manamgoda et al. 2012 JX276455 Manamgoda et al. 2012
Curvularia sp. ICMP 13910 JX256445 Manamgoda et al. 2012 JX276456 Manamgoda et al. 2012
C. microspora sp.nov GUCC 6272 MF139088 This study MF139106 This study MF139097 This study MF139115 This study
C. microspora sp. nov GUCC 6273 MF139089 This study MF139107 This study MF139098 This study MF139116 This study
C. microspora sp. nov GUCC 6274 MF139090 This study MF139108 This study MF139099 This study MF139117 This study
C. microspora sp. nov GUCC 6275 MF139091 This study MF139109 This study MF139100 This study MF139118 This study
C. microspora sp. nov GUCC 6276 MF139092 This study MF139110 This study MF139101 This study MF139119 This study
C. microspora sp. nov GUCC 6277 MF139093 This study MF139111 This study MF139102 This study MF139120 This study
C. microspora sp. nov GUCC 6278 MF139094 This study MF139112 This study MF139103 This study MF139121 This study
C. microspora sp. nov GUCC 6279 MF139095 This study MF139113 This study MF139104 This study MF139122 This study
C. microspora sp. nov GUCC 6280 MF139096 This study MF139114 This study MF139105 This study MF139123 This study

Pathogenicity test

Pathogenicity of this species was determined by inoculating healthy leaves of Hippeastrum striatum and Canna indica L. with 5 mm diameter mycelial plugs, cut from the margins of 10-day-old actively growing cultures; the control was treated with sterile agar plugs. Both inoculated and control plants were kept in a moist chamber at 25 °C for 7 days and observed for disease symptom development. Infected leaves were collected and the fungus was re-isolated in PDA medium and compared against the original strains. Control plants were sprayed with sterilised distilled water.

Results

Phylogenetic analyses

Nine isolates of Curvularia were sequenced from two plants in Chongqing Municipality, China (seven from Hippeastrum striatum and two from Canna indica). PCR products of approximately 900 bp (28S), 540 bp (ITS), 530 bp (GPD1) and 1200 bp (TEF1) were obtained. In the molecular phylogenetic analyses, the partition homogeneity test (P = 0.06) indicated that the individual partitions were not highly incongruent (Cunningham 1997) and thus 28S, ITS, GPD1 and TEF1 sequences were combined for sequence analyses. By alignment with a single gene region and then combination according to the order of 28S, ITS, GPD1 and TEF1, only 2689 characters were obtained, viz. 28S: 1–848, ITS: 849–1330, GPD1: 1331–1771 TEF1: 1772–2689 with 104 parsimony-informative characters and 157 parsimony-uninformative characters. The analysis produced three equally parsimonious trees, one of which (TL = 366, CI = 0.81, RI = 0.82, RC = 0.66 and HI = 0.19) is shown in Figure 1 and the topologies of MP and ML analysis were congruent, thus only MP topology was shown. Phylogenetic analysis confirmed nine strains (GUCC 6272, GUCC 6273, GUCC 6274, GUCC 6275, GUCC 6276, GUCC 6277, GUCC 6278, GUCC 6279 and GUCC 6280) with the same DNA sequences in four phylogenetic markers grouped into an independent clade supported by high bootstrap values (MP: 100%; ML: 99%). These strains were placed in trifolii-clade with strong bootstrap support (MP: 95%; ML: 95%) and had a close relationship with Curvularia gaudauskasii, C. gladioli, C. trifolii, C. borreriae and C. pallescens with a high MP support (MP: 87%), but its ML bootstrap value was lower than 50%.

Figure 1. 

The only one parsimonious tree obtained from combined analyses set of ITS, LSU,β-tubulin and tef1 sequence data. MP values (>50 %) resulting from 1000 bootstrap replicates. The tree is rooted with Alternaria alternata (EGS 34-0160). The branch of our new Curvularia is shown in blue.

Taxonomy

Curvularia microspora Y. Liang, K.D. Hyde, J. Bhat & Yong Wang, sp. nov.

MycoBank No: 822544
Figure 2

Diagnosis

Characterised by producing four celled, smaller conidia (4.5–11.5 × 2–6 µm), usually curved at the third cell from the base.

Type

China, Chongqing City, Nanchuan, from leaf spots of Hippeastrum striatum, 28 September 2016, Y. Liang, HGUP 6272, holotype, ex-type living culture GUCC 6272.

Description

Symptoms on Hippeastrum striatum: Fructification mostly epiphyllous, disease spot 3–12 mm, subspherical to oblong ovate, brown to dark brown, effuse (Figure 2a, b). Symptoms on Canna indica: Fructification of the fungus was mostly epiphyllous, the large blighted, irregular spots near leaf apex to the whole leaves, greyish-brown (Figure 2c).

Colonies on PDA, vegetative hyphae septate, branched, subhyaline to brown, smooth to asperulate, 1.5–3 µm, anastomosing. Sexual morph: Undetermined. Asexual morph: Hyphomycetous. Conidiophores 10.5–77.5 × 1–3.5 µm (av. = 22.2 × 2.1 µm, n = 30), arising singly, simple or branched, flexuous, septate, geniculate at spore bearing part, pale brown, dark brown, paler towards apex. Percurrent proliferation only observed occasionally. Conidiogenous loci somewhat thickened and darkened, spores up to 0.8–1 µm diam, smooth. Mature conidia always four celled, 4.5–11.5 × 2–6 µm (av. = 8.2 × 3.8 µm, n = 50), smooth-walled, usually curved at the third cell from the base, sometimes straight, navicular, bifurcate, obpyriform, tapering towards rounded ends, pale brown to dark reddish brown. Hilum usually conspicuous or sometimes slightly protuberant.

Habitat and distribution

Isolated from leaf diseases of H. striatum and Canna indica in China

Etymology

microspora, referring to this species producing obviously smaller conidia.

Other material examined

China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6273), living culture GUCC 6273; China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6274), living culture GUCC 6274; China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6275), living culture GUCC 6275; China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6276), living culture GUCC 6276; China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6277), living culture GUCC 6277; China, Chongqing City, Nanchuan, from leaf diseases of H. striatum, 28 September 2016, Y. Liang (HGUP 6278), living culture GUCC 6278; China, Chongqing City, Nanchuan, from leaf diseases of Canna indica, 28 September 2016, Y. Liang (HGUP 6279), living culture GUCC 6279; China, Chongqing City, Nanchuan, from leaf diseases of C. indica, 28 September 2016, Y. Liang (HGUP 6280), living culture GUCC 6280.

Pathogenicity test

Test plants (Hippeastrum striatum) were inoculated with 5 mm diam mycelial plugs of Curvularia microspora with two replicates of each plants and the inoculation experiment was repeated two times (with different sporulation generations). Hippeastrum striatum leaves both exhibited brown to dark brown necrotic spots (Figure 3a, b) after 7 days, which were very similar to those of natural infection (Figure 2a, b). The DNA sequencing result (ITS region), after re-isolation, identified this as C. microspora. The successful re-isolation of C. microspora from the inoculated leaves of H, striatum established a credible proof of pathogenicity. All test plants were covered with polyethylene bags for 7 days. However, on Canna indica, disease symptoms did not appear again.

Figure 2. 

Curvularia microspora (HGUP 6272). a–c Leaf diseases symptoms on Hippeastrum rutilum and Canna indica. d–f Conidiophores, conidiogenous loci and conidia g–j Immature and mature conidia k–l Upper (k) and lower (l) surface of colony. Scar bars: d, i (10 μm), e–f = 20μm, g–h, j = (5 μm).

Figure 3. 

Curvularia microspora inoculated to Hippeastrum rutilum (7 days). a the first time for inoculation b the second time for inoculation.

Discussion

The nine strains of Curvularia had typical characters of the genus., viz. the production of sympodial conidiophores with tretic, terminal and intercalary conidiogenous cells and elongate, transversely septate conidia with a dark basal scar (Boedijn 1933). Phylogenetic analyses compared the DNA sequence from four phylogenetic markers with related species in the trifolii-clade: Curvularia akaii, C. borreriae, C. gladioli, C. gaudauskasii, C. heteropogonis, C. pallescens and C. trifolii (Figure 1, Manamgoda et al. 2012, 2015, Madrid et al. 2014, Jeong et al. 2015, Su et al. 2015). These taxa are morphologically similar in producing a strongly protruding hilum (Madrid et al. 2014). However, the present taxon had bifurcate conidia, which differentiates it from all other species in the trifolii-clade. Curvularia microspora also has smaller conidia than the related species. A synopsis of the characters in the trifolii-clade is given in Table 2. The phylogenetic analyses (MP and ML) also confirmed these isolates belong to a new taxon with strong bootstrap support (Figure 1).

Morphological comparison and pathogenecity of Curvularia microspora and related species in trifolii-clade.

Species name Taxonomic references Conidia Conidiophores Pathogenecity Pathogenic reports
Shape Size range
Curvularia microspora This study curved at the third cell from the base, sometimes straight, navicular, bifurcate, obpyriform, tapering towards rounded ends 4.5–11.5 × 2.0–6.0 µm 10.5–77.5 × 1.0–3.5 µm Yes This study
Curvularia akaii Tsuda and Ueyama (1985) 24–34 × 8.7–13.8 µm Yes Zhang (2004)
Curvularia borreriae Ellis (1971) 20–32 × 8–15 µm No
Curvularia gladioli Boerema and Hamers (1989) 17.5–37.5 × 6.5–17.5 µm Yes Horita (1995); Torres et al. (2013, 2015)
Curvularia gudauskasii Morgan-Jones and Karr Jr (1976) 27–29 × 15–19 µm 62–98 × 5–6 µm Yes Chinea (2005); Ratón et al. (2012)
Curvularia heteropogonis Alcorn (1990) 27–44 × 11–19 µm 115–620 × 4–6 µm Yes Alcorn (1990)
Curvularia pallescens Ellis (1971) 17–32 × 7–12 µm Yes Berg et al. (1995); Dadwal and Verma (2009); Mabadeje (1969); Rajalakshmy (1976)
Curvularia trifolii Groves and Skolko (1945) 20–34 × 8–14 µm Yes Falloon (1976); Khadka (2016); Sarwar and Srinath (1965); Sung et al. (2016); Zamorski (1983);

Curvularia species can cause severe or opportunistic diseases of different plant taxa and are often a threat to agricultural production by reducing yield and quality. In the trifolii-clade, all species except for C. borreriae, have been reported as causing plant disease. This is especially true of C. trifolii and C. pallescens, which cause serious diseases of Agrostis stolonifera and Gloriosa superba respectively (Table 2). Koch’s postulates were performed to show that C. microspora causes leaf spot disease of Hippeastrum striatum (Figure 3), but on Canna indica might only be saprobic or endophytic. Hippeastrum striatum as an economic ornamental plant is grown in some areas of China, thus there is a need to continue investigation on the biology of this species in order to determine whether it can cause serious disease outbreaks.

Acknowledgments

The research is supported by the project of National Natural Science Foundation of China (No. 31560489), National Key Technology Research and Development Programme of the Ministry of Science and Technology of China (2014BAD23B03/03), Genetically Modified Organisms Breeding Major Projects of China [2016ZX08010-003-009], Agriculture Animal and Plant Breeding Projects of Guizhou Province [QNYZZ2013-009], Fundamental Research on Science and Technology, Ministry of Science and Technology of China (2014FY120100), postgraduate education innovation programme of Guizhou Province (ZYRC[2014]004) and Bijie science and technology project No. (2015)39.

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