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Boeremia tuber rot of sweet potato caused by B. exigua , a new postharvest

storage disease in China

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DOI: 10.1080/07060661.2016.1158742

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 Canadian Journal of Plant Pathology

ISSN: 0706-0661 (Print) 1715-2992 (Online) Journal homepage: http://www.tandfonline.com/loi/tcjp20

Boeremia tuber rot of sweet potato caused by

B. exigua, a new post-harvest storage disease in
China

Yun-Peng Gai, Hai-Jie Ma, Xing-Long Chen, Hao-Hao Chen & Hong-Ye Li

To cite this article: Yun-Peng Gai, Hai-Jie Ma, Xing-Long Chen, Hao-Hao Chen & Hong-
Ye Li (2016) Boeremia tuber rot of sweet potato caused by B.�exigua, a new post-harvest
storage disease in China, Canadian Journal of Plant Pathology, 38:2, 243-249, DOI:
10.1080/07060661.2016.1158742

To link to this article: https://doi.org/10.1080/07060661.2016.1158742

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Mar 2016.
Published online: 23 Mar 2016.

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Can. J. Plant Pathol., 2016
Vol. 38, No. 2, 243–249, http://dx.doi.org/10.1080/07060661.2016.1158742

Disease reports/Rapport des maladies

Boeremia tuber rot of sweet potato caused by B. exigua, a new

post-harvest storage disease in China

YUN-PENG GAI1, HAI-JIE MA1, XING-LONG CHEN2, HAO-HAO CHEN1 AND HONG-YE LI1

1
Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China
2
Department of Plant Pathology, College of Agriculture and Biotechnology, China Agricultural University, Beijing 100193, P.R. China

(Accepted 22 February 2016)

Abstract: A new post-harvest storage disease was observed on sweet potato (Ipomoea batatas L.) in Zhejiang Province, China in November
2014. A species of Boeremia was constantly isolated from diseased tissues with typical symptoms of storage tuber rot. The isolates were
identified as Boeremia exigua based on morphological characteristics and phylogenetic analyses of the internal transcribed spacer (ITS) region
and 5.8S ribosomal DNA, the 28S large subunit ribosomal RNA (LSU) gene, the β-tubulin (TUB) gene and the actin (ACT) gene. The
pathogenicity of the fungal isolates was confirmed through inoculation experiments. This is the first report of Boeremia tuber rot caused by B.
exigua on sweet potato in China.

Keywords: Boeremia exigua, Boeremia tuber rot, Ipomoea batatas, sweet potato

Résumé: Une nouvelle maladie postculturale de conservation a été observée chez la patate douce (Ipomoea batatas L.) dans la province du
Zhejiang, en Chine, en novembre 2014. Une espèce de Boeremia a été continuellement isolée à partir de tissus infectés affichant les symptômes
typiques de la pourriture d’entrepôt chez les tubercules. En se basant sur les caractéristiques morphologiques et les analyses phylogénétiques
de la région de l’espaceur transcrit interne (ITS) de l’ADN et de l’ADN ribosomal 5.8S, de la grande sous-unité (GSU) du gène de l’ARN
ribosomal 28S, du gène de la β-tubuline (TUB) et du gène de l’actine (ACT), les isolats ont été identifiés en tant que Boeremia exigua. La
pathogénicité des isolats fongiques a été confirmée par des expériences d’inoculation. Il s’agit de la première mention de la pourriture du
tubercule causée par B. exigua sur la patate douce en Chine.

Mots clés: Boeremia exigua, Ipomoea batatas, patate douce, pourriture d’entrepôt, pourriture du tubercule causée par Boeremia

Introduction Sweet potato is affected by approximately 100 biotic and

abiotic diseases (Clark & Moyer 1988). Several of these
Sweet potato, Ipomoea batatas L., a member of the
diseases are considered post-harvest diseases, such as
Convolvulaceae family, is an important root crop in
Rhizopus soft rot caused by Rhizopus stolonifer
China, and is cultivated over 4.1 million hectares with
(Ehrenb.) Vuill. and R. arrhizus A. Fisch., Java black
an annual production of 100 million tonnes and average
rot caused by Botryodiplodia theobromae Pat., and
productivity of 24.4 tonnes ha−1 (Loebenstein &
Fusarium stem canker caused by Fusarium solani
Thottappilly 2009). China is the largest producer of
(Mart.) Sacc. (Clark & Moyer 1988). These post-harvest
sweet potato in the world, with 48% of the cultivated
diseases are mostly detected after harvest and severe
area and 70% of the total worldwide production (Qin
losses are more common in warmer regions
et al. 2014). Sweet potato is beneficial to humans because
(Loebenstein & Thottappilly 2009).
of its high content of dietary fibre, nutrients and minerals.

Correspondence to: Y. P. Gai. E-mail: gaiy@zju.edu.cn

© 2016 The Canadian Phytopathological Society

Published online 23 Mar 2016

Y.-P. Gai et al.
Boeremia exigua (Desm.) Aveskamp, Gruyter &
Verkley is a ubiquitous, necrotrophic pathogen with a
broad host range and worldwide occurrence (Boerema
& Höweler 1967). The species and varieties of
Boeremia have a complicated taxonomic history and pre-
viously belonged to the Phoma genus. Aveskamp et al.
(2010) reclassified several species of Phoma in the new
genus Boeremia based on their ostiole morphology. Nine
varieties of B. exigua are proposed based on phenotypic
characters and molecular genetic analysis (Van der Aa
et al. 2001; De Gruyter et al. 2002). The most well known
variety, B. exigua var. exigua, has been reported to infect
over 200 plant hosts, causing diseases such as leaf blight,
leaf spot, stem rot, stem blight, and post-harvest rots of
fleshy roots and tubers (Koike et al. 2006). The other B.
exigua varieties and their primary hosts are the following:
B. exigua var. linicola on Linum usitatissimum L., B.
exigua var. forsythiae on Forsythia sp., B. exigua var.
heteromorpha on Nerium oleander L., B. exigua var.
populi on Populus euramericana (Dode) Guinier, B. exi-
gua var. pseudolilacis on Syringa vulgaris L., B. exigua
var. viburni on Viburnum opulus L., B. exigua var. for-
sythiae on Forsythia sp., B. exigua var. lilacis on Syringa
vulgaris L. (Aveskamp et al. 2010).
During November and December 2014, an unidentified
disease of sweet potato was observed in a modern refrig-
eration storage lot in Hangzhou, Zhejiang Province,
China. The sweet potato tubers were harvested by local
growers in Jinyun, Zhejiang, China in 2014. The disease
symptoms differed from previously occurring bacterial or
fungal diseases of sweet potato in China or elsewhere in
the world. The aim of this study was to identify the causal
agent of this disease.
Materials and methods
Isolation and characterization of the pathogen
Fifty kg of diseased tubers were sampled from a storage
lot in Hangzhou, Zhejiang, China. Symptomatic sections
of diseased tuber were excised, surface sterilized with 1%
sodium hypochlorite solution for 1 min, and rinsed three
Table 1. Details of isolates used in this study.
Species Isolate No. Host
Boeremia exigua var. exigua ZJUB106 Ipomoea batatas
ZJUB107 Ipomoea batatas
ZJUB108 Ipomoea batatas
ZJUB: Boeremia strains collected in Zhejiang University.
244
times in sterile distilled water. Excised tissue (<5 mm3)
from the junctions of healthy and necrotic areas were
incubated on potato dextrose agar (PDA) supplemented
with 100 mg L−1 streptomycin sulphate at room tempera-
ture. The cultures were purified using the hyphal-tip
method and maintained on PDA for cultural, morpholo-
gical and pathological studies. Isolates used in this study
are listed in Table 1. For morphological identification, a
mycelial disc (8 mm) taken from the margin of 5-day-old
actively growing colonies were placed in the centre of
PDA, oatmeal agar (OA) and malt extract agar (MEA) in
90 mm diameter Petri dishes and incubated at 25 ± 1°C
for 21 days (Aveskamp et al. 2009a). Cultural character-
istics were observed, colony diameters were measured,
and the conidial morphology was recorded.
Morphological characteristics of the fungi growing on
culture media were examined using differential interfer-
ence contrast microscopy (Eclipse 80i, Nikon, Japan),
and photographed using a Nikon digital camera (NIS-
Elements F3.0, Nikon, Japan). The shape, length and
width of 50 conidia were measured at 400× magnifica-
tion. The presence of antibiotic E was tested by placing a
drop of concentrated NaOH on the edge of 7-day-old
colonies grown on MEA and observing any colour
changes (Boerema & Höweler 1967; Boerema et al.
2004).
Pathogenicity test
Inoculum of three isolates was prepared by growing them
on PDA for 2 weeks. A small hole of 5 mm in diameter and
10 mm deep was made on sweet potato tubers ‘Nongfu’
with a sterile cork borer. Agar plugs of the fungal isolates
were placed in the hole with individual tubers being inocu-
lated with individual fungal isolates. There were 30 inocu-
lated tubers for each isolate. Control sweet potato tubers
were inoculated with sterile agar plugs. Inoculated tubers
were incubated at 25 ± 2°C on the greenhouse bench and the
relative humidity was 85–95% in a greenhouse. All sweet
potato tubers were examined after 1 month, and sweet
potato tubers with necrotic lesions and typical symptoms
Origin LSU ITS TUB ACT
Zhejiang, China KR653195 KR653198 KR653201 KR653204
Zhejiang, China KR653196 KR653199 KR653202 KR653205
Zhejiang, China KR653197 KR653200 KR653203 KR653206
Boeremia tuber rot of sweet potato in China 245

of grey to dark brown tuber rot were analysed for the with a bootstrap of 1000 replicates (Tamura et al. 2007).
presence of fungi as described above. The experiment was Phoma herbarum strain CBS 615.75 was used as an out-
conducted twice. group taxon for this analysis.

Molecular identification Results and discussion

Mycelia of the fungus were collected from 5-day-old cul- Symptoms of the disease
tures grown in 50 mL of liquid yeast extract peptone dex-
trose medium (yeast extract 10 g, peptone 20 g, dextrose The disease was observed in storage at a moderate to high
20 g, water 1000 mL) in 150 mL flasks at 25oC. Mycelia severity and the percentage of infected tubers was 80%.
were filtered first and about 0.3 g of fresh mycelia were Sweet potato tubers may initially appear healthy with the
transferred to 2 mL centrifuge tubes, centrifuged, and fungus present as a latent infection, but damage due to rough
washed twice with sterile water. Genomic DNA was handling during lifting, grading or processing, or due to low
extracted from the mycelium using a Biospin Fungus temperatures, can activate the fungus to cause tuber dry rot,
Genomic DNA Extraction Kit (Bio-Flux, Bioer particularly during storage. The storage temperature was 8–
Technology Co., China). The internal transcribed spacer 12°C and the relative humidity was 88–92%. The disease
(ITS) regions and 5.8S ribosomal DNA were amplified first appeared as small, round, dark grey to black lesions on
using the primers V9G and ITS4 (White et al. 1990; Hoog tubers. These lesions enlarged and formed circular to irre-
& Ende 1998) (Table 2). The 28S large subunit ribosomal gularly shaped lesions. The infected portion of the sweet
RNA (LSU) gene was amplified using LROR and LR7 potato showed a clear and distinct margin between healthy
primers (Vilgalys & Hester 1990; Rehner & Samuels and affected tissue (Fig. 1a–b). Ultimately, the disease
1994). The β-tubulin (TUB) gene was amplified with the caused internal rot beneath the superficial lesions, which
primers Btub2Fd and Btub4Rd (Aveskamp et al. 2009a).
The actin (ACT) gene was amplified with the primers ACT-
512F and ACT-783R (Carbone & Kohn 1999).
Amplification was carried out in a S1000TM Thermal
Cycler (Bio-Rad Laboratories, Germany). The PCR primers
and annealing temperature are listed in Table 2. PCR-ampli-
fied products were electrophoresed on 1.5% agarose gels
and purified using QIAquick PCR purification Kit (Qiagen)
and sequenced at Invitrogen (Life Technologies, Shanghai,
China) in both directions and consensus sequences
assembled. Resultant sequences were compared with refer-
ence isolates deposited within the GenBank database of the
National Centre for Biotechnology Information using
BLASTN with default settings. The sequences of represen-
tative isolates were deposited into GenBank (Table 1).
Fig. 1 (Colour online) Disease symptoms caused by Boeremia
Sequences were aligned using the multiple sequence align- exigua on sweet potato. a–b, Dark grey to black lesions on storage
ment program, Clustal W (Chenna et al. 2003) and the tuber of sweet potato. c–d, Dark purple to brown internal dry rot
phylogenetic analysis was performed using MEGA 4.0 beneath the superficial lesions.

Table 2. The primers used in this study.

Loci Primer Primer sequences Annealing temperature (°C) Reference

ITS V9G 5′-TTA CGT CCC TGC CCT TTG TA-3′ 48 (Hoog & Ende 1998)
ITS4 5′-TCC TCC GCT TAT TGA TAT GC-3′ (White et al. 1990)
LSU LROR 5′-ACC CGC TGA ACT TAA GC-3′ 48 (Rehner & Samuels 1994)
LR7 5′-TAC TAC CAC CAA GAT CT-3′ (Vilgalys & Hester 1990)
TUB Btub2Fd 5′-GTB CAC CTY CAR ACC GGY CAR TG-3′ 52 (Aveskamp et al. 2009a)
Btub4Rd 5′-CCR GAY TGR CCR AAR ACR AAG TTG TC-3′
ACT ACT-512F 5′-ATG TGC AAG GCC GGT TTC GC-3′ 55 (Carbone & Kohn 1999)
ACT-783R 5′-TAC GAG TCC TTC TGG CCC AT-3′
Y.-P. Gai et al.
was characterized by dark purple to brown dry rots
(Fig. 1c–d).
Identification and characterization of the pathogen
One type of fungus was consistently isolated from
symptomatic tubers of sweet potato. A total of three
morphologically indistinguishable isolates (ZJUB106,
ZJUB107 and ZJUB108) were obtained in this study
(Table 1). The isolate ZJUB108 was used as a repre-
sentative isolate for species identification. The fungus
grown on PDA had irregular margins, lime green to
dark greyish with white felty aerial mycelia (Fig. 2a–b).
Colonies on PDA were 32–36 mm in diameter after
7 days and 55–62 mm after 14 days. On MEA, colonies
had irregular margins and appeared grey to dark brown
with white to cream aerial mycelia. Colonies were 40–
48 mm in diameter after 7 days and 72–75 mm after
14 days (Fig. 2c). On OA, colonies had irregular mar-
gins and appeared lime grey to dark grey with younger
white aerial mycelia. Colonies on OA had diameters of
52–58 mm after 7 days and all colonies reached the
edges of Petri dishes after 14 days (Fig. 2d). Pycnidia
and conidia were readily formed on the media. Conidia
were ellipsoid to oblong, or almost cylindrical, with
rounded ends, measured (5.1)–6.6–(8.1) × (2.4)–3.0–
(3.3) µm with a length/width (L/W) ratio of 2.2 ± 0.3
(Fig. 3a–b). Adding drops of NaOH to the edges of
actively growing isolates on MEA did not result in any
Fig. 2 (Colour online) Cultures of B. exigua isolate ZJUB108 (left surface side, right reverse side) from sweet potato. a, 7-day-old cultures on
potato dextrose agar. b, 3-week-old cultures on potato dextrose agar. c, 3-week-old cultures on malt extract agar. d, 3-week-old cultures on
oatmeal agar.
246
colour changes to the medium indicating that antibiotic
E was not present. The isolate ZJUB108 was identified
as Boeremia exigua (Desm.) Aveskamp, Gruyter &
Verkley based on morphological characters.
Pathogenicity test
Necrotic lesions and typical symptoms of grey to dark
brown tuber rot were visible on inoculated sweet potato
tubers within 30 days compared with non-inoculated con-
trols (Fig. 3c–d). All three isolates used in pathogenicity
test were pathogenic to sweet potato. Affected sweet
potato tubers failed to sprout. Disease symptoms were
similar to symptoms noted on naturally infected diseased
tubers. A fungus similar to the original isolates was
reisolated from all symptomatic tissues by the same iso-
lation method and was confirmed to be Boeremia exigua.
The control tubers remained healthy, and results of the
two experiments were similar.
Molecular identification
Previously, species and varieties in B. exigua complex
were delineated using two fingerprint techniques:
Amplified Fragment Length Polymorphism (AFLP)
and DAF (DNA Amplification Fingerprinting) using
mini-hairpin primers (Aveskamp et al. 2009b). The
morphological identification of the isolates in the pre-
sent study was confirmed with molecular analyses
Boeremia tuber rot of sweet potato in China 247

Fig. 3 (Colour online) The pathogen and inoculation test. a, Mycelia of B. exigua isolate ZJUB108. b, Conidia of isolate ZJUB108. c–d,
Reproduction of the natural symptoms after inoculation with isolate ZJUB108.

Table 3. Information on molecular identification of the fungal isolates in this study.

Isolate Gene GenBank accession GenBank number of reference Sequence length Identity Reference isolate
code region number isolate (bp) (%) Fungal species code

ZJUB108 LSU KR653197 EU754182 1309 100.0% Boeremia exigua var. CBS 101150
exigua
ZJUB108 ITS KR653200 EU343118 703 99.7% B. exigua var. exigua CBS 118.94
ZJUB108 TUB KR653203 KT389780 333 99.7% B. exigua var. linicola CBS 248.38
ZJUB108 TUB KR653203 GU237499 333 99.7% B. exigua var. linicola CBS 114.28
ZJUB108 TUB KR653203 FJ427112 341 99.1% B. exigua var. exigua CBS 431.74
ZJUB108 ACT KR653206 EU880878 224 100.0% B. exigua var. linicola CBS 112.28
ZJUB108 ACT KR653206 EU880877 224 100.0% B. exigua var. linicola CBS 109.49
ZJUB108 ACT KR653206 EU880869 224 99.6% B. exigua var. CBS 443.94
heteromorpha
ZJUB108 ACT KR653206 EU880846 224 99.1% B. exigua var. exigua CBS 101151

LSU = 28S large subunit ribosomal RNA; ITS = internal transcribed spacer; TUB = beta-tubulin; ACT = actin.

using multiple loci. The LSU, ITS, TUB and ACT loci
sequence data of three isolates (ZJUB106, ZJUB107
and ZJUB108) generated in this study have been
deposited in GenBank and the accession numbers are
listed in Table 1. The sequences amplified from the
LSU, ITS, TUB and ACT were 99–100% identical to
B. exigua var. exigua and B. exigua var. linicola
(Table 3). Sequences of LSU, ITS, TUB and ACT
regions were combined for each strain as these genes
have been shown to be highly effective in resolving
species in the genus Boeremia (Aveskamp et al. 2010).
The four concatenated sequences of three isolates
(ZJUB106, ZJUB107 and ZJUB108), 11 strains of B.
exigua, two strains of B. foveata, and two strains of B.
telephii were used in the phylogenetic analysis and
isolate CBS 615.75 of Phoma herbarum as an out-
group. This united dataset comprised 2418 characters
after alignment. In the maximum parsimony analysis,
2289 characters were constant, 104 were parsimony
uninformative, and 25 were parsimony informative.
The tree constructed from LSU, ITS, TUB and ACT
sequences clustered all B. exigua into a single clade
rooted to an outgroup species Phoma herbarum CBS
615.75. Phylogenetic analyses revealed that all three
Y.-P. Gai et al.
Fig. 4 Phylogenetic tree of B. exigua isolates from sweet potato in China and other Boeremia species using NJ analysis of combined LSU,
ITS, TUB and ACT nucleotide sequences. The bootstrap support values higher than 50% from 1000 replicates are shown at the nodes. The tree
is rooted with Phoma herbarum.
isolates in this study were identical to each other and
grouped in a single clade and closely related to B.
exigua var. linicola (Fig. 4).
Previous reports have shown that B. exigua and B.
foveata are major pathogens causing gangrene and tuber
rot on potato (Solanum tuberosum L.) worldwide
(Giebel & Dopierała 2004; Cimmino et al. 2008).
Unlike the specific gangrene pathogen B. foveata, B.
exigua is known as a broad host range fungus, and has
been isolated from more than 200 host genera world-
wide. To the best of our knowledge, this is the first
report of Boeremia tuber rot caused by B. exigua on
sweet potato. We studied the disease and its pathogen
based on the disease symptoms, morphological and
molecular phylogeny. Inoculation tests of the fungal
isolates were carried out to the same host to fulfil
Koch’s postulates. We propose the name ‘Boeremia
tuber rot of sweet potato’ for the newly recognized
disease of sweet potato. Inoculation tests indicate this
pathogen can rapidly colonize the tubers of sweet
potato, demonstrating its potential to cause significant
losses. No effective control strategy has yet been estab-
lished. Fortunately, this disease was only observed dur-
ing storage of sweet potato and has not been found in
commercial fields. However, as China is the largest
sweet potato producer in the world, this disease may
pose a threat to sweet potato production.
248
Acknowledgements
This study was supported by the Student Research
Training Programme of Zhejiang University of China
(Project Number: 2015032199). We thank Xin Liu and
Jingwen Lv, Zhejiang University, for technical assistance
and Dr Feng Huang, Zhejiang University, for constructive
comments on an earlier draft of the manuscript.
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