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

Soft rot of potatoes caused by Bacillus

amyloliquefaciens in Guangdong province, China

Li Wang, Xiao-Bo Li, Hai-Cui Suo, Kang An, Huan-Min Luo & Xiao-Jin Liu

To cite this article: Li Wang, Xiao-Bo Li, Hai-Cui Suo, Kang An, Huan-Min Luo & Xiao-Jin Liu
(2017) Soft rot of potatoes caused by Bacillus amyloliquefaciens in Guangdong province, China,
Canadian Journal of Plant Pathology, 39:4, 533-539, DOI: 10.1080/07060661.2017.1381994

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 Can. J. Plant Pathol., 2017
Vol. 39, No. 4, 533–539, https://doi.org/10.1080/07060661.2017.1381994

Disease Report/Rapport des maladies

Soft rot of potatoes caused by Bacillus amyloliquefaciens in

Guangdong province, China

LI WANG#, XIAO-BO LI#, HAI-CUI SUO, KANG AN, HUAN-MIN LUO AND XIAO-JIN LIU

Research Institute of Crops, Provincial Key Laboratory of Crops Genetic Improvement, Guangdong Academy of Agricultural Sciences,
Guangzhou, Guangdong, 510640, P.R. China

(Accepted 16 September 2017)

Downloaded by [wang li] at 04:24 06 November 2017

Abstract: Potato tubers exhibiting symptoms of soft rot were observed in a field in Baiyun District, Guangzhou, Guangdong Province, China,
in March 2016. Bacteria were isolated from the diseased potato tubers. Using morphological and molecular (16S rDNA and gyrB)
characterization and pathogenicity tests, a representative isolate of the bacterium was identified as Bacillus amyloliquefaciens. Inoculating the
isolate onto healthy potato tubers led to soft rot with the same symptoms as displayed in the field, which confirmed Bacillus amyloliquefaciens
as the causal agent. Further testing of the bacterial isolate on other hosts showed that it could also cause soft rot on tomato, onion and pepper.
To our knowledge, this is the first report of soft rot of potato tubers caused by Bacillus amyloliquefaciens in the field.

Keywords: Potato, soft rot, Solanum tuberosum, tubers

Résumé: En mars 2016, on a observé des tubercules de pommes de terre affichant des symptômes de pourriture molle dans un champ du
district de Baiyun, à Guangzhou, dans la province du Guangdong, en Chine. Des bactéries ont été isolées des tubercules infectés. En se basant
sur la caractérisation morphologique et moléculaire (ADNr 16S et gyrB) ainsi que sur des tests de pathogénicité, un isolat représentatif de la
bactérie a été identifié en tant que Bacillus amyloliquefaciens. L’inoculation de tubercules de pomme de terre sains avec l’isolat a engendré la
pourriture molle présentant les symptômes semblables à ceux trouvés au champ, ce qui a permis de confirmer que Bacillus amyloliquefaciens
était bien l’agent causal. D’autres tests menés avec l’isolat de la bactérie sur d’autres hôtes ont montré qu’il pouvait également causer la
pourriture molle chez la tomate, l’oignon et le poivron. À notre connaissance, il s’agit de la première mention de pourriture molle chez la
pomme de terre causée par Bacillus amyloliquefaciens en champ.

Mots clés: Pomme de terre, pourriture molle, Solanum tuberosum, tubercules

Introduction
out during the winter cropping season, starting in late
Potato (Solanum tuberosum L.) is the fourth most autumn (late October/November) and ending in spring
important food crop in the world after wheat, rice and (February/March of the following year), filling the gap
corn (Zaheer & Akhtar 2016). China is the world’s between summer rice cropping seasons. This unique
largest potato producer, accounting for 25% of world cropping system (from a paddy field crop to a dry-
output. Cultivation occurs in the subtropical provinces, land crop in one year) enables the same field to pro-
such as Guangdong and Guangxi, to the far north-east duce rice in the summer and potatoes in the early
regions, including Heilongjiang and Inner Mongolia. spring. It not only provides the main staple food
Potato production in southern China is mainly carried crop, rice, but also supplies the spring market with

Correspondence to: Xiao-Jin Liu. E-mail: [email protected]

#
Li Wang and Xiao-Bo Li contributed equally to this study.

© 2017 The Canadian Phytopathological Society

 L. Wang et al. 534

fresh potatoes. Clearly, potato production in southern colony from an isolate was selected and transferred into
China plays a significant role in China’s potato 2.0 mL NA medium, cultured in a shaking incubator (200
industry. rpm) at 30°C for 24 h and then centrifuged at 12 000 rpm
The crop quality and potato tuber yield are affected by for 10 min. After removing the supernatant, the bacteria
diseases caused by fungal, bacterial and viral pathogens at pellet was suspended in 100 µL 10× TE buffer and incu-
various stages of growth and development. Potato soft rot bated in boiling water for 10 min. Thereafter, the sample
disease occurs worldwide. It can be caused by several was centrifuged at 12 000 rpm for 5 min, and the resulting
pathogens, including species of Enterobacteriaceae (such supernatant, containing the DNA, was used for PCR.
as Pectobacterium atrosepticum, P. carotovorum subsp. car-
otovorum, P. carotovorum subsp. brasiliense, P. wasabiae
Molecular identification of the pathogen
and P. parmentieri) (Gardan et al. 2003; Zhang et al. 2012;
Des Essarts et al. 2016; Suárez et al. 2017), Dickeya (such The 16S rDNA gene, which is commonly used for bac-
as Dickeya dianthicola, D. dadantii, D. zeae and D. solani) terial identification, was targeted. The DNA fragment was
(Czajkowski et al. 2015; Ranjan et al. 2016) and amplified by PCR using the universal bacteria primers
Pseudomonas marginalis (Li et al. 2007). The disease is 27F (5´-AGAGTTTGATCMTGGCTCAG-3´) and 1492R
often associated with excessive moisture and high tempera- (5´-TACGGYTACCTTGTTACGACTT-3´) (Amann et al.
tures, and can occur during the later growth period in the 1995). The 20 µL PCR reaction mixture contained 1 µL
field and during storage after harvest. In March 2016, potato DNA suspension, 0.25 µL of TaKaRa rTaq (5 U µL−1)
Downloaded by [wang li] at 04:24 06 November 2017

tubers exhibiting soft rot disease were observed in a winter (TaKaRa, Dalian, China), 1.6 µL dNTP mixture (2.5 mM
potato crop field on potato cultivar ‘YueHong 1’ in the each) and 0.5 µm each of forward and reverse universal
Baiyun District (23°8′33′′N, 113°17′34′′E), Guangzhou, primers. PCR was performed on a DNA thermal cycler
Guangdong province of China, during the harvest period. (PC320; ASTEC, Fukuoka, Japan) with an initial dena-
The exterior of the infected tubers showed shrivelled skins turation at 94°C for 3 min, followed by 35 cycles at 94°C
that could be stripped off easily, while the inside of the for 30 s, 55°C for 30 s and 72°C for 1 min 40 s, with a
tubers was slimy and had a sour rot smell (Fig. 1a,b). The final elongation step at 72°C for 5 min. Amplified frag-
disease occurred with an incidence of ~3–5% of all tubers in ments were separated on a 1.5% agarose gel by electro-
the field. The objective of this study was to identify and phoresis, collected from the gel and purified using a DNA
characterize the causal agent causing potato soft rot in the quick purification kit (TaKaRa, Dalian, China) according
winter potato crop in Guangdong province, China. to the manufacturer’s instructions. The purified amplicons
were cloned into the pMDTM18-T vector using a vector
cloning kit (TaKaRa, Dalian, China) following the man-
Materials and methods ufacturer’s instructions. Three positive clones of each
Isolation of the pathogen isolate were sequenced using the universal M13F and
M13R primer set by Sangon Biotech (Shanghai, China).
Eight potato tubers with soft rot symptoms were collected In addition, the partial sequence of DNA gyrase subunit
from a potato field in the Baiyun District, Guangdong B gene (gyrB) was also amplified by the primer set gyrB-
Province, China. The symptomatic tubers were first washed F (5´-TTGRCGGHRGYGGHTATAAAGT-3´)/gyrB-R (5
with running water, followed by a rinse with sterile water. ´-TCCDCCSTCAGARTCWCCCTC-3´) (Wang et al.
The diseased tissues were cut into small pieces (about 2013) using the procedure described above, except the
20 × 20 mm), dipped into 70% ethanol for 30 s, and 0.1% 72°C extension was only 1 min. The resulting PCR
mercuric chloride for 2 min, followed by 3–5 rinses with amplicons were cloned and sequenced as described
sterile water. The surface-sterilized tissues were homoge- above. Representative sequences were deposited in the
nized in a sterile mortar containing 2 mL sterile distilled GenBank database. The newly obtained sequences above
water. The suspension was then streaked onto nutrient agar of 16S rDNA and gyrB were analysed using a BLAST
(NA) using an inoculating loop and incubated at 28 ± 1°C algorithm-based program (https://blast.ncbi.nlm.nih.gov/
for 48 h, and the prevalent bacterial colonies were subcul- Blast.cgi) to identify the bacterial isolates.
tured onto NA plates for purification.
Morphological and biochemical characterizations
Genomic DNA extraction
Colony morphology was observed after growing for
To identify the bacteria obtained from the plates, genomic 2 days on NA agar. Microscopic morphological charac-
DNA was extracted from representative isolates. Briefly, a teristics were observed using a phase contrast
 Potato soft rot caused by Bacillus amyloliquefaciens 535
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Fig. 1 (Colour online) Symptoms of soft rot of potato tubers and morphological characteristics of B. amyloliquefaciens. Exterior (a) and
interior (b) symptoms of soft rot of potato tubers in the field; Colony (c) and cell (d) morphology of B. amyloliquefaciens. Exterior (e) and
interior (f) symptoms of potato tubers inoculated with B. amyloliquefaciens.

microscope (40×) (AxioScope A1, Zeiss, Germany). instructions. The analyses were performed using
The Gram-staining reaction was performed using the Apiweb software (version 4.0; bioMérieux).
method described by Nugent et al. (1991). Biochemical
characteristics were determined using the bioMerieuxTM
Phylogenetic analysis
APITM system (Bio-Mérieux, Marcy L’Etoile, France)
with API 50CHB strips that are usually used to identify In addition to the newly obtained sequences, closely
genus Bacillus strains following the manufacturer’s related sequences of type strain retrieved from the
 L. Wang et al. 536

EzTaxon-e (http://www.ezbiocloud.net/) (Kim et al. Results and discussion

2012) and GenBank databases (https://www.ncbi.nlm.
Isolation and morphological characterization of the
nih.gov/genbank/) were included for phylogenetic ana-
pathogen
lysis. The sequences of 16S rDNA and gyrB genes of
Bacillus sp. were independently aligned using ClustalW Eight bacterial isolates with similar colony morphologies
1.83. The Neighbour-joining trees were constructed were isolated from eight symptomatic potato tubers. The
using MEGA version 7.0, using the Kimura 2-para- isolate colonies were creamy-white, non-translucent, with
meter model method, and bootstrap values were based surface folding and had irregular margins on NA plates
on 1000 replications (Kumar et al. 2016). (Fig. 1c). Cells were short rods ranging in size from 0.64
to 0.72 μm in width and 1.38 to 2.31 μm in length
Pathogenicity tests (Fig. 1d). These characteristics are consistent with those
described for the genus Bacillus.
Eight bacterial isolates from different tubers were
grown on NA plates for ~36 h at 30°C and used as
inoculum for pathogenicity tests on potato and other Biochemical and molecular identification of the pathogen
plant species, including tomato, onion and green pep- The bacterial cells were Gram-stain positive. The isolates
per. For tests on potato, three healthy potato tubers of had positive reactions in the following tests: glycerol,
cultivar ‘YueHong 1’ were inoculated with the bacterial L-rabinose, D-ribose, D-xylose, D-glucose, S-fructose,
Downloaded by [wang li] at 04:24 06 November 2017

isolates using the needle-stab inoculation method S-mannose, inositol, L-mannitol, L-sorbitol, methyl α-D-
described by Lan et al. (2013) with slight modifica- glucoside, amygdalin, arbutin, esculin/ferric citrate, salicin,
tions. Briefly, healthy tubers were stabbed with a ster- D-cellobiose, L-maltose, D-lactose, D-melibiose,
ilized toothpick to a depth of 0.5 cm at one location on D-trehalose, D-melezitose, D-raffinose, Amidon, glycogen,
their surfaces and a drop of bacterial suspension con- gentiobiose; and had negative reactions in the following
taining 108 cfu mL−1 (10 µL) was placed on the wound tests: erythritol, D-arabinose, L-xylose, D-adonitol, Methyl
sites. The tubers were maintained in an incubator at β-D-xylopyranoside, D-galactose, L-sorbose, L-rhamnose,
30°C in darkness at 95% humidity for 3–5 days. dulcitol, methyl α-D-mannoside, N-acetyl-glucosamine,
Negative control tubers were inoculated with sterile Inulin, D-melezitose, Xylitol, D-turanose, D-lyxose,
distilled water as described above. The pathogenicity D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol,
of the bacterial isolates on tomato, onion and green potassium gluconate, potassium 2-ketogluconate, potassium
pepper were also tested by inoculation as described 5-ketogluconate (Table 1). The biochemical properties of
above. The experiment was repeated three times to the isolates showed 94.7% consistency with that of Bacillus
confirm the results. subtilis and B. amyloliquefaciens in the database of the

Table 1. Biochemical characterization of bacterial isolates causing soft rot of potato tubers using API 50CHB.
Test Result Test Result Test Result

Glycerol + L-mannitol + D-raffinose +

Erythritol − L-sorbitol + Amidon +
D-arabinose − methyl α-D-mannoside - glycogen +
L-rabinose + methyl α -D-glucoside + Xylitol −
D-ribose + N-acetyl-glucosamine - gentiobiose +
D-xylose + amygdalin + D-turanose −
L-xylose − arbutin + D-lyxose −
D-adonitol − esculin/ferric citrate + D-tagatose −
Methyl β-D-xylopyranoside − salicin + D-fucose −
D-galactose − D-cellobiose + L-fucose −
D-glucose + L-maltose + D-arabitol −
S-fructose + D-lactose + L-arabitol −
S-mannose + D-melibiose + potassium gluconate −
L-sorbose − D-saccharose + potassium 2-ketogluconate −
L-rhamnose − D-trehalose + potassium 5-ketogluconate −
dulcitol − Inulin −
inositol + D-melezitose −

+ positive reaction, – negative reaction.

 Potato soft rot caused by Bacillus amyloliquefaciens 537

a 96 F10-1 (KY773617)
85 B. amyloliquefaciens subsp. plantarum FZB42 T (CP000560)
B. amyloliquefaciens subsp. amyloliquefaciens DSM 7 T (FN597644)
B. vallismortis DV1-F-3 T (AB021198)
B. subtilis subsp. spizizenii NRRL B-23049 T (CP002905)
100 71 B. subtilis DSM10T (AJ276351)
B. subtilis subsp. inaquosorum DSM 22148 T (HE582781)
90
B. atrophaeus JCM9070(AB021181)
B. sonorensis NRRL B-23154 T (AF302118)
100 B. aerius 24K T (AJ831843)
88 99
B. licheniformis DSM13 T (X68416)

99 B. pumilus ATCC7061 T (AY876289)

B. safensis DSM 19292 T (AF234854)

100 B. stratosphericus 41KF2a T (AJ831841)

B. aerophilus 28K T (AJ831844)
99
B. altitudinis DSM 21631 T (AJ831842)
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57 B. humi LMG22167 T (AJ627210)

B. herbersteinensis D-1,5a T (AJ781029)
51 B. pakistanensis KCTC 13786T T (AB618147)
71 B. acidicola 105-2 T (AF547209)
P. azotofixans P3L-5T (AJ251192)

0.01

b 80 B. subtilis subsp. spizizenii BCRC 17366 T (DQ309299).

90 B. subtilis subsp. subtilis BCRC 10255 T (DQ309293).
99
B. subtilis subsp. inaquosorum NRRL B-23052 T (HQ605914)
100
B. vallismortis BCRC 17183 T (DQ309298)
86 B. mojavensis BCRC 17124 T (DQ309297)
B. amyloliquefaciens subsp. amyloliquefaciens DSM 7 T (FN597644)
89 F10-1(KY829110)
100
100 B. amyloliquefaciens subsp. plantarum FZB42 T (CP000560)
92
B. atrophaeus BCRC 17123 T (DQ309296)
B. licheniformis BCRC 11702 T (DQ309295)
100 B. sonorensis BCRC 17416 T (DQ309300)
B. safensis DSM 19292 T (AY167867)
100 B. altitudinis DSM 21631 T (JX680219)
B. cereus ATCC 14579 T (AB190226)

0.05

Fig. 2 Neighbour-joining tree showing the phylogenetic positions of the strain F10-1 and other related taxa based on 16S rRNA (a) and gyrB
(b) gene sequences. Paenibacillus azotofixans P3L-5T (AJ251192) and Bacillus cereus ATCC 14 579T (AB190226) were used as outgroups,
respectively. Bootstrap support values resulted from 1000 replicates. Bootstrap values below 50% are not shown.
 L. Wang et al. 538

Apiweb software (bioMérieux), suggesting that the bacterial healthy potato tubers. The tubers inoculated with the isolates
isolates are likely to be B. subtilis or B. amyloliquefaciens. each showed similar symptoms. At 24 h after inoculation,
To further identify the isolates, amplicons corresponding to the inoculation sites started to rot and sink slightly. Over
the 16S rDNA and gyrB genes were cloned and sequenced time, the soft rot enlarged in both diameter and especially in
from eight isolates. The 16S rDNA and gyrB amplicons were depth. Six days after inoculation, the inoculation sites
1514 bp and 986 bp in length, respectively. The sequence exuded a yellow liquid. Cutting longitudinally into the
alignment indicated that all of the respective 16S rDNA and tubers revealed that the rotting had spread from the inocula-
gyrB sequences from the eight isolates were identical, indi- tion sites to most of the tissues, resulting in the entire tuber
cating that the isolates had the same origin. Thus, one repre- being soft and rotten, with a slimy texture and a rotten odour
sentative isolate, designated F10-1, was chosen for further (Fig. 1e,f). In contrast, no visible symptoms developed
study. The sequences of the 16S rDNA and gyrB of F10-1 either externally or internally on control tubers inoculated
were submitted to GenBank (accession nos KY773617 and with sterile distilled water. Thus, F10-1 is confirmed to be
KY829110, respectively). A BLAST algorithm-based analy- the causal agent leading to the soft rot of potatoes in a field
sis indicated that the sequences shared 99–100% and 99% in Guangdong, China.
identities with the 16S rDNA and gyrB, respectively, reported Previously, B. amyloliquefaciens was reported as the
for Bacillus amyloliquefaciens strains. causal agent of bacterial soft rot in onion in Korea
(Hwang et al. 2012) and arrowhead (Sagittaria sagitti-
folia) during storage in China (Zhong et al. 2015). The
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Phylogenetic analysis
present research not only reveals that B. amyloliquefa-
Phylogenetic trees were constructed based on the 16S rDNA ciens is a new causal agent of bacterial soft rot in
and gyrB gene sequences. Paenibacillus azotofixans P3L-5T potato, but it also demonstrates the ability of the bac-
(AJ251192) and Bacillus cereus ATCC 14579T(AB190226) terium to induce soft rot in several important horticul-
sequences were used as outgroups in the analyses, respec- tural crops, including tomato, green pepper and onion
tively. In the 16S rDNA tree, the representative isolate F10-1 (Fig. 3). To our knowledge, this is the first report of B.
was grouped together with B. amyloliquefaciens subsp. plan- amyloliquefaciens causing potato soft rot disease in a
tarum FZB42T (CP000560), and B. amyloliquefaciens subsp. potato production field. This new soft rot strain/isolate
amyloliquefaciens DSM 7T (FN597644) (Fig. 2a), all of of B. amyloliquefaciens can cause serious losses (~5%)
which belong to B. amyloliquefaciens. In the gyrB tree, of potato crops.
F10-1 also clustered with B. amyloliquefaciens subsp. plan- Bacillus amyloliquefaciens is also a potential antago-
tarum FZB42 T (CP000560) and B. amyloliquefaciens subsp. nist for the control of several fungal diseases on some
amyloliquefaciens DSM 7T (FN597644) (Fig. 2b). Thus, crops (Xu et al. 2014; Chen et al. 2016). The identifica-
F10-1 was confirmed to be an isolate of B. amyloliquefaciens. tion of the soft rot-causing strains/isolates of B. amyloli-
quefaciens in potato (this study) as well as in onion
(Hwang et al. 2012) and S. sagittifolia (Zhong et al.
Pathogenicity test
2015) suggests that the F10-1 isolate may be a new
To determine whether the isolates are capable of inducing pathogenic strain of B. amyloliquefaciens but further
soft rot in potato, the eight isolates were inoculated onto research is needed to confirm this.

Fig. 3 (Colour online) Disease symptoms on tomato (a), pepper (b) and onion (c) inoculated with B. amyloliquefaciens.
 Potato soft rot caused by Bacillus amyloliquefaciens 539

Acknowledgements Gardan L, Gouy C, Christen R, Samson R. 2003. Elevation of three

subspecies of Pectobacterium carotovorum to species level:
We thank Dr Yunpeng Gai from Zhejiang University for Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum
constructive comments on an earlier draft of the sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Micr.
53:381–391.
manuscript. Hwang SK, Back CG, Win NKK, Kim MK, Kim HD, Kang IK, Lee
SC, Jung HY. 2012. Occurrence of bacterial rot of onion caused by
Bacillus amyloliquefaciens in Korea. J Gen Plant Pathol. 78:227–232.
Funding Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS,
Lee JH, Yi H, et al. 2012. Introducing EzTaxon-e: A prokaryotic 16S
This study was supported by the Science and Technology rRNA gene sequence database with phylotypes that represent uncultured
Planning Project of Guangdong Province [grant number species. Int J Syst Evol Microbiol. 62:716–721.
2016A020209004, 2017B020201005, 2017A020208033, Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary
2017A020208021]; Technology Research and Development genetics analysis version 7.0 for bigger datasets. Mol Biol Evol.
33:1870–1874.
Subsidies Project of Department of Finance of Guangdong Lan WW, Nishiwaki Y, Akino S, Kondo N. 2013. Soft rot of root
Province to YueCaiGong in 2015 [grant number 639]; chicory in Hokkaido and its causal bacteria. J Gen Plant Pathol.
Modern Agricultural Science and Technology Innovation 79:182–193.
Alliance Construction Project of Guangdong Province Li J, Chai Z, Yang H, Li G, Wang D. 2007. First report of Pseudomonas
marginalis pv. marginalis as a cause of soft rot of potato in China.
[grant number 2016LM3163]; Scientific Research Special Austral Plant Dis Notes. 2:71–73.
Fund of Public Welfare Industry (Agriculture) [grant number Nugent RP, Krohn MA, Hillier SL. 1991. Reliability of diagnosing
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201503123-03]; Modern Agricultural Science and bacterial vaginosis is improved by a standardized method of gram stain
Technology Innovation Alliance Construction Project of interpretation. J Clin Microbiol. 29:297–301.
Ranjan R, Singh D, Baranwal V. 2016. Simultaneous detection of brown
Guangdong Province [2016LM3163]; Technology Research rot and soft rot-causing bacterial pathogens from potato tubers through
and Development Subsidies Project of Department of Finance multiplex PCR. Curr Microbiol. 73:652–659.
of Guangdong Province to YueCaiGong in 2015 [639]; Suárez MB, Feria FJ, Martín-Robles MJ, del Rey FJ, Palomo JL.
2017. Pectobacterium parmentieri causing soft rot on potato tubers in
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