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Identification of Lasiodiplodia Pseudotheobromae Causing Fruit

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Identification of Lasiodiplodia Pseudotheobromae Causing Fruit plants Brief Report Identification of Lasiodiplodia pseudotheobromae Causing Fruit Rot of Citrus in China Jianghua Chen 1,2, Zihang Zhu 1, Yanping Fu 1,2, Jiasen Cheng 1, Jiatao Xie 1 and Yang Lin 1,* 1 Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, Wuhan 430070, China; [email protected] (J.C.); [email protected] (Z.Z.); [email protected] (Y.F.); [email protected] (J.C.); [email protected] (J.X.) 2 National R & D Center for Citrus Postharvest Technology, Huazhong Agricultural University, Wuhan 430070, China * Correspondence: [email protected]; Tel.: +86-27-87280487 Abstract: Considering the huge economic loss caused by postharvest diseases, the identification and prevention of citrus postharvest diseases is vital to the citrus industry. In 2018, 16 decayed citrus fruit from four citrus varieties—Satsuma mandarin (Citrus unshiu), Ponkan (Citrus reticulata Blanco cv. Ponkan), Nanfeng mandarin (Citrus reticulata cv. nanfengmiju), and Sugar orange (Citrus reticulata Blanco)—showing soft rot and sogginess on their surfaces and covered with white mycelia were collected from storage rooms in seven provinces. The pathogens were isolated and the pathogenicity of the isolates was tested. The fungal strains were identified as Lasiodiplodia pseudotheobromae based on their morphological characteristics and phylogenetic analyses using the internal transcribed spacer regions (ITS), translation elongation factor 1-α gene (TEF), and beta-tubulin (TUB) gene sequences. The strains could infect wounded citrus fruit and cause decay within two days post inoculation, but could not infect unwounded fruit. To our knowledge, this is the first report of citrus fruit decay caused by L. pseudotheobromae in China. Keywords: citrus; fruit decay; Lasiodiplodia pseudotheobromae Citation: Chen, J.; Zhu, Z.; Fu, Y.; Cheng, J.; Xie, J.; Lin, Y. Identification of Lasiodiplodia pseudotheobromae Causing Fruit Rot of Citrus in China. 1. Introduction Plants 2021, 10, 202. https://doi.org/ Citrus is the second-largest fruit crop in China. It is cultivated in over 20 provinces, 10.3390/plants10020202 with an area of approximately 2.5 million ha [1,2]. China has an over 4000-year history of citrus cultivation. There are an abundant and excellent variety of resources in China. Received: 4 December 2020 Fruit decay is a common disease during postharvest transportation and storage. Generally, Accepted: 19 January 2021 the decay rate is 20% to 30%, and sometimes it can reach up to 50%, which causes serious Published: 21 January 2021 postharvest economic losses [3]. Therefore, disease control is vital for the postharvest period of citrus fruit. Publisher’s Note: MDPI stays neutral Common postharvest citrus diseases include green mold, blue mold, sour rot, an- with regard to jurisdictional claims in thracnose, Diplodia stem-end rot, Diaporthe stem-end rot, brown rot, and Alternaria published maps and institutional affil- stem-end rot, etc. In 2018, a survey of postharvest citrus diseases in storage rooms found iations. that the average fruit decay rate exceeded 30% in seven provinces. In addition to the common postharvest diseases, 16 decayed fruit showing soft rot and soggy lesions with dense white hyphae were also observed. In this study, the causal agent of the citrus fruit rot disease was determined via morphological observation, molecular identification, and Copyright: © 2021 by the authors. pathogenicity tests. Licensee MDPI, Basel, Switzerland. This article is an open access article 2. Results distributed under the terms and 2.1. Fungal Isolates conditions of the Creative Commons Attribution (CC BY) license (https:// In 2018, a total of 2402 citrus fruit from four different citrus varieties (Satsuma man- creativecommons.org/licenses/by/ darin (Citrus unshiu), Ponkan (Citrus reticulata Blanco cv. Ponkan), Nanfeng mandarin 4.0/). (Citrus reticulata cv. nanfengmiju), and Sugar orange (Citrus reticulata Blanco)) were taken Plants 2021, 10, 202. https://doi.org/10.3390/plants10020202 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 9 2. Results 2.1. Fungal Isolates Plants 2021, 10, 202 In 2018, a total of 2402 citrus fruit from four different citrus varieties (Satsuma2 of 8 mandarin (Citrus unshiu), Ponkan (Citrus reticulata Blanco cv. Ponkan), Nanfeng manda- rin (Citrus reticulata cv. nanfengmiju), and Sugar orange (Citrus reticulata Blanco)) were fromtaken storage from storage houses houses (15 ◦C) (15 in seven°C) in provincesseven provinces (Guangxi, (Guangxi, Hubei, Zhejiang,Hubei, Zhejiang, Hunan, Hunan, Jiangxi, Fujian,Jiangxi, andFujian, Guangdong) and Guangdong) and investigated. and investigated. Except for Except fruit with for fruit typical with green typical mold green and bluemold mold and symptoms,blue mold 402symptoms, diseased 402 fruit diseased samples fruit were samples collected were for fungal collected isolation. for fungal From theisolation. 402 decayed From fruit,the 402 450 decayed fungal strains fruit, 450 were fungal isolated. strains Based were on theisolated. morphological Based on char- the acteristicsmorphological and internalcharacteristics transcribed and internal spacer regionstranscribed (ITS) spacer sequences, regions most (ITS) of themsequences, were identifiedmost of them as Geotrichum were identifiedspp., Colletotrichumas Geotrichum spp., DiplodiaColletotrichumspp., Alternariaspp., Diplodiaspp., spp., etc. Al- In addition,ternaria spp., 16 strains etc. In belonging addition, to 16 the strains genus belongingLasiodiplodia towere the genus also isolated Lasiodiplodia from 16 were diseased also fruitsisolated with from soft, 16 water-soaked diseased fruits lesions with soft, (Figure water-soaked1a, Table1). lesions (Figure 1a, Table 1). Figure 1. Symptoms of of the the diseased diseased fruit fruit and and colony colony morphology morphology on on potato potato dextrose dextrose agar agar (PDA). (PDA). ((a)) SymptomsSymptoms of the diseased citrus citrus fruit. fruit. ( (bb)) Colony Colony morphology morphology of of the the fungal fungal strains strains JX.1, JX.1, GD.2, GD.2, and HN.3 on PDA incubated at at 25 25 °C◦C in in the the dark dark for for 2 2 days; days; (c (c) )Colony Colony morphology morphology of of the the fungal fungal strains JX.1, GD.2,GD.2, andand HN.3HN.3 onon PDAPDA incubatedincubated atat 3535 ◦°CC in the dark for 40 days. Table 1. Samples used in this study. No. of Rotten Fruit Except for Lasiodiplodia Total No. of Citrus Varieties Location Those with Green Incidence (%) Strain Investigated Fruit and Blue Mold Symptoms Guangxi, Guilin 1 27 225 0.44 Hunan, Huaihua 5 76 320 1.56 Citrus unshiu Hubei, Wuhan 1 69 258 0.39 Hubei, Yicang 1 18 344 0.29 Zhejiang, Taizhou 2 20 259 0.77 Citrus reticulata Fujiang, Quanzhou 1 7 92 1.09 Blanco cv. Ponkan Citrus reticulata cv. Jiangxi, Nanfeng 3 111 566 0.53 nanfengmiju Citrus reticulata Guangdong, 2 74 338 0.59 Blanco Quangzhou Plants 2021, 10, 202 3 of 8 2.2. Molecular Characterization Based on the multiple gene analyses, 16 strains were identified as Lasiodiplodia pseu- dotheobromae. A MegaBlast analysis showed that they exhibited 100% identity to the type Plants 2021, 10, x FOR PEERstrain REVIEW of L. pseudotheobromae (CBS 116459). Since the 16 strains were of the4 of 9 same species, three of2.2. them Molecular from Characterization different citrus varieties and producing areas—JX.1, GD.2, and HN.3— were randomlyBased selectedon the multiple for further gene analyses, study (Table16 strains S1). were In total,identified 1727 as charactersLasiodiplodia of 62 isolates from 30pseudotheobromaeLasiodiplodia. Aspecies MegaBlast and analysis one outgroup showed that species they exhibited (Diplodia 100% seriataidentity) to were the used to con- struct Maximumtype strain of likelihood L. pseudotheobromae (ML) and(CBS Maximum116459). Since Parsimony the 16 strains (MP) were phylogeneticof the same trees. The species, three of them from different citrus varieties and producing areas—JX.1, GD.2, combinedand HN.3—were data included randomly 525 charactersselected for further of ITS study (1–525), (Table 550S1). In characters total, 1727 characters of translation elonga- tion factorof 62 1- isolatesα gene from (TEF 30) Lasiodiplodia (530–1079), species and 643and one characters outgroup of species beta-tubulin (Diplodia seriata (TUB) ) (1085–1727). Based onwere the used MP to construct analysis, Maximum a single likelihood most parsimonious (ML) and Maximum tree Parsimony was constructed (MP) phy- (tree length (TL) = 460,logenetic consistency trees. The combined index (CI) data = included 0.654, retention525 characters index of ITS (RI) (1–525), = 0.854, 550 characters rescaled consistency of translation elongation factor 1-α gene (TEF) (530–1079), and 643 characters of be- index (RC)ta-tubulin = 0.559, (TUB) homoplasy(1085–1727). Based index on the (HI) MP =analysis, 0.346). a single Of all most the parsimonious characters, tree 175 characters were parsimonywas constructed informative, (tree length (TL) 63 variable= 460, consistency characters index (CI) were = 0.654, parsimony retention index uninformative, (RI) and 1,489 characters= 0.854, rescaled were consistency consistent. index (RC) The = topology 0.559, homoplasy of the index ML (HI) tree = 0.346). was similarOf all the to that of the MP tree.characters, The isolates 175 characters were groupedwere parsimony with informative,L. pseudotheobromae 63 variable charactersbut were were distinguished par- from simony
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