Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (4): 719-728.doi: 10.3864/j.issn.0578-1752.2022.04.008

• PLANT PROTECTION • Previous Articles     Next Articles

Proliferation of Two Types Prophage of ‘Candidatus Liberibacter asiaticus’ in Diaphorina citri and their Pathogenicity

HUANG JiaQuan1(),LI Li1,WU FengNian2,ZHENG Zheng1,DENG XiaoLing1()   

  1. 1College of Plant Protection, South China Agricultural University, Guangzhou 510642
    2School of Life Sciences and Food Engineering, Hanshan Normal University, Chaozhou 521041, Guangdong
  • Received:2021-07-14 Accepted:2021-08-13 Online:2022-02-16 Published:2022-02-23
  • Contact: XiaoLing DENG E-mail:380794041@qq.com;xldeng@scau.edu.cn

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Abstract:

【Background】In China, citrus Huanglongbing is a destructive disease associated with ‘Candidatus Liberibacter asiaticus’ (CLas), which currently threatening the sustainable development of citrus industry. Previous studies had identified three types of prophage sequences in the genome of CLas strains. Prophage group typing analysis revealed that the Type 2 prophage strains and Type 1+3 prophage strains dominated in Guangdong Province. However, the difference in propagation capacity of these two strains of CLas in Asian citri psyllid (Diaphorina citri) and pathogenicity of these two strains leading by insect transmission remains unknown. 【Objective】The objective of this study is to assess the difference in proliferation capacity between Type-2-CLas and Type-1+3-CLas in D. citri and the pathogenicity variations between them on Citrus reticulata Blanco cv. Shatangju. 【Method】The buds with different strains of CLas were grafted to healthy Shatangju. Fifty nymphal and fifty adult D. citri were caged on the young shoots of infected Shatangju to acquire different strains of CLas for 6, 12, and 18 days, respectively. Real-time quantitative PCR (qPCR) was used to detect and analyze the difference in the acquisition rate and quantity of Type-2-CLas and Type-1+3-CLas between the nymphal stage and the adult stage of D. citri. Further, twenty adult D. citri infected with Type-2-CLas or Type-1+3-CLas were placed on the young shoots of healthy Shatangju to inoculate for two weeks, respectively. The D. citri were collected and detected by qPCR. The general information of infection rate and quantity of CLas was collected. Symptom development of Shatangju and titers of CLas in leaves were monitored each month. Morphological change of leaves phloem and parenchyma cell was visualized by light microscopy 360 days after inoculation. 【Result】There was no significant difference between acquisition rate and quantity of Type-2-CLas and Type-1+3-CLas detected in D. citri that fed on the infected plant at the nymphal stage. In contrast to fed as nymphs, the acquisition rate and quantity of Type-2-CLas were significantly higher than Type-1+3-CLas when D. citri fed on infected plant at the adult stage. The leaves presented more severe mottled symptom after inoculation with Type-2-CLas at 120 d after D. citri removal. The immature leaves at young shoots had an obstacle on turning green, presenting leathery, small size, and yellowing which was infected with Type-2-CLas. The symptoms on Type-1+3-CLas infected plants were presented as typical mottled leaves and leathery. Anatomical analyses indicated that Type-2-CLas caused more severe damage to phloem and accumulated more starch in parenchyma cell even if the titer of Type-1+3-CLas was closed to Type-2-CLas. 【Conclusion】Compared to Type-1+3-CLas, Type-2-CLas was more capable of invading and proliferating in adult D. citri, accompanied by a higher titer of CLas which indirectly proved the high contagious capacity of Type-2-CLas. The young leaves infected with Type-2-CLas presented symptoms of uniform yellowing, small size, while infected with Type-1+3-CLas showed lightly mottled and leathery. Type-2-CLas destroyed more phloem cells and caused severe starch accumulation, indicating that Type-2-CLas had stronger pathogenicity to citrus than Type-1+3-CLas.

Key words: citrus Huanglongbing, ‘Candidatus Liberibacter asiaticus’ (CLas), prophage, Diaphorina citri, pathogenicity

Table 1

General information of the specific real-time qPCR primer sequences"

引物名称
Primer name		 引物序列
Primer sequence (5′→ 3′)		 目的基因
Target gene		 引物特异性
Specificity		 来源
Source
SC1-gp060F TCGCTCTCCTTCAAATTGCG 假设蛋白
Hypothetical protein		 Type 1 本研究This study
SC1-gp060R GTTTTAGTCCCGTCCGATGC
SC2-gp045F ACATCAGAGGCTACATCGGG 假设蛋白
Hypothetical protein		 Type 2 本研究This study
SC2-gp045R ACGTCTCGGTGGCTTAAAGA
P-JXGC-8F CGGCGCTGAACTCTTGTATT R-M system Type 3 文献[10] Reference [10]
P-JXGC-8R AAGGGCGTTGTTCTTGTCAC
CLas-4G AGTCGAGCGCGTATGCGAAT 16S rRNA gene 16S rRNA gene 文献[24] Reference [24]
HLBr GCGTTATCCCGTAGAAAAAGGTAG
HLBp FAM-AGACGGGTGAGTAACGCG-BHQ

Table 2

Acquisition rate and quantity of different strains of CLas feeding by D. citri at different life stages"

刺吸时间
Access period		 样本数量
Number of samples		 获菌率
Acquisition rate (%)		 单头木虱平均CLas数量
Mean CLas counts of individual D. citri
Type 1+3 Type 2 Type 1+3 Type 2 Type 1+3 Type 2
若虫期刺吸 Access as nymph
6 d A 28 27 39.26±3.23a 70.37±3.70a 6.01×104 ±1.62×104a 6.98×104±2.31×104a
12 d 29 28 74.44±10.94b 80.83±10.83a 9.18×105±2.73×105b 3.58×106±1.81×106b
18 d 32 32 82.16±13.55b 93.33±6.67a 1.09×106±4.04×105b 7.99×105±1.57×105b
成虫期刺吸 Access as adult
6 d 28 30 10.00±0a 20.00±0a 3.65×104±1.64×103a 5.01×104±4.24×103a
12 d 30 28 20.00±0b 30.00±0b 2.46×104±4.50×103a 4.59×106±1.27×106b
18 d 30 30 23.33±3.33b 43.33±3.33c 2.38×104±8.24×103a 4.84×104±1.34×104a

Table 3

Infection status of citrus caused by different strains of CLas after D. citri transmission"

菌株类型
Strains type		 植株编号
Tree No.		 柑橘木虱存活率
D. citri survival
rate (%)		 柑橘木虱获菌率
D. citri acquisition rate (%)		 CLas-4G-qPCR的Ct值 Ct values of CLas-4G-qPCR
0 d 60 d 120 d 360 d
D. citri FL FL FL/NFL YFL
Type 1+3 CCT1-1 80.00 100.00 22.01±0.46 37.63±0.35 19.70±0.31 20.69±0.09 21.22±0.11
CCT1-2 85.00 100.00 22.18±0.46 38.95±0.56 19.80±0.32 19.49±0.12 22.15±0.10
CCT1-3 60.00 100.00 21.25±0.48 39.25±0.69 19.52±0.21 20.59±0.08 23.31±0.09
CCT1-4 80.00 100.00 22.28±0.67 38.56±0.58 19.32±0.09 20.64±0.08 21.33±0.01
CCT1-5 95.00 100.00 21.44±0.50 38.45±0.62 19.82±0.14 21.43±0.10 24.22±0.20
CCT1-6 90.00 100.00 21.89±0.45 39.25±0.84 34.06±0.32 20.23±0.09 21.65±0.06
CCT1-7 80.00 100.00 22.84±0.35 38.65±0.98 20.52±0.07 22.57±0.16 21.19±0.11
CCT1-8 65.00 100.00 21.92±0.38 37.87±0.48 18.56±0.11 20.36±0.07 22.37±0.09
Type 2 CCT2-1 95.00 100.00 22.26±0.91 38.69±0.52 24.38±0.13 21.40±0.12 22.53±0.09
CCT2-2 85.00 94.12 22.30±1.08 38.35±0.68 35.76±0.22 28.77±0.11 23.39±0.14
CCT2-3 75.00 100.00 21.05±0.61 39.25±0.86 34.46±0.11 23.67±0.09 22.52±0.06
CCT2-4 70.00 100.00 22.75±1.53 38.26±0.75 23.53±0.06 22.40±0.15 22.51±0.09
CCT2-5 70.00 50.00 23.31±2.45 37.65±0.36 36.48±0.19 21.64±0.16 22.21±0.07
CCT2-6 55.00 100.00 21.86±1.10 39.65±0.78 39.77±0.23 21.58±0.06 23.29±0.18
CCT2-7 90.00 88.89 25.00±1.25 38.36±0.81 23.56±0.05 22.53±0.18 22.17±0.10
CCT2-8 50.00 20.00 25.74±1.65 37.84±0.71 36.53±0.09 34.50±0.19 28.35±0.25

Fig. 1

Symptom variations of Huanglongbing caused by different strains of CLas"

Fig. 2

Anatomical analyses of midrib and mesophyll tissues infected with different strains of CLas"

[1] BOVÉ J M. Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, 2006, 88(1):7-37.
[2] JAGOUEIX S, BOVÉ J M, GARNIER M. The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. International Journal of Systematic Bacteriology, 1994, 44(3):379-386.
doi: 10.1099/00207713-44-3-379
[3] 邓晓玲, 唐伟文. 应用PCR技术检测柑桔黄龙病病原的研究. 华南农业大学学报, 1996, 17(3):119-120.
DENG X L, TANG W W. The studies on detection of citrus Huanglongbing pathogen by polymerase chain reaction. Journal of South China Agricultural University, 1996, 17(3):119-120. (in Chinese)
[4] 林孔湘. 柑桔黄梢(黄龙)病研究Ⅰ-病情调查. 植物病理学报, 1956, 2(1):1-11.
LIN K X. Observation on yellow shoots disease of citrus. Acta Phytopathologica Sinica, 1956, 2(1):1-11. (in Chinese)
[5] ZHENG Z, CHEN J, DENG X. Historical perspectives, management, and current research of citrus HLB in Guangdong Province of China, where the disease has been endemic for over a hundred years. Phytopathology, 2018, 108(11):1224-1236.
doi: 10.1094/PHYTO-07-18-0255-IA
[6] ZHANG S, FLORES-CRUZ Z, ZHOU L, KANG B H, FLEITES L A, GOOCH M D, WULFF N A, DAVIS M J, DUAN Y P, GABRIEL D W. ‘Ca. Liberibacter asiaticus’ carries an excision plasmid prophage and a chromosomally integrated prophage that becomes lytic in plant infections. Molecular Plant-Microbe Interactions, 2011, 24(4):458-468.
doi: 10.1094/MPMI-11-10-0256
[7] ZHENG Z, BAO M, WU F, VAN HORN C, CHEN J, DENG X. A type 3 prophage of ‘Candidatus Liberibacter asiaticus’ carrying a restriction-modification system. Phytopathology, 2018, 108(4):454-461.
doi: 10.1094/PHYTO-08-17-0282-R
[8] DAI Z, WU F, ZHENG Z, YOKOMI R, KUMAGAI L, CAI W, RASCOE J, POLEK M, CHEN J, DENG X. Prophage diversity of ‘Candidatus Liberibacter asiaticus’ strains in California. Phytopathology, 2019, 109(4):551-559.
doi: 10.1094/PHYTO-06-18-0185-R
[9] 李嘉慧, 郑正, 邓晓玲. 基于原噬菌体类型的我国柑橘黄龙病菌种群遗传结构分析. 植物病理学报, 2019, 49(3):334-342.
LI J H, ZHENG Z, DENG X L. Population genetic structure of ‘Candidatus Liberibacter asiaticus’ in China based on the prophage types. Acta Phytopathologica Sinica, 2019, 49(3):334-342. (in Chinese)
[10] ZHENG Y, HUANG H, HUANG Z, DENG X, ZHENG Z, XU M. Prophage region and short tandem repeats of ‘Candidatus Liberibacter asiaticus’ reveal significant population structure in China. Plant Pathology, 2021, 70(4):959-969.
doi: 10.1111/ppa.v70.4
[11] JAIN M, FLEITES L A, GABRIEL D W. Prophage-encoded peroxidase in ‘Candidatus Liberibacter asiaticus’ is a secreted effector that suppresses plant defenses. Molecular Plant-Microbe Interactions, 2015, 28(12):1330-1337.
doi: 10.1094/MPMI-07-15-0145-R
[12] FLEITES L A, JAIN M, ZHANG S, GABRIEL D W. ‘Candidatus Liberibacter asiaticus’ prophage late genes may limit host range and culturability. Applied and Environmental Microbiology, 2014, 80(19):6023-6230.
doi: 10.1128/AEM.01958-14
[13] 范国成, 刘波, 吴如健, 李韬, 蔡子坚, 柯冲. 中国柑橘黄龙病研究30年. 福建农业学报, 2009, 24(2):183-190.
FAN G C, LIU B, WU R J, LI T, CAI Z J, KE C. Thirty years of research on citrus Huanglongbing in China. Fujian Journal of Agricultural Sciences, 2009, 24(2):183-190. (in Chinese)
[14] 许长藩, 夏雨华, 李开本, 柯冲. 柑桔木虱传播黄龙病的规律及病原在虫体内分布的研究. 福建农业学报, 1988, 3(2):57-62.
XU C F, XIA Y H, LI K B, KE C. Studies on the law of transmission of citrus Huanglongbing by psyllid, Diaphorina citri and the distribution of pathogen in the adult. Fujian Journal of Agricultural Sciences, 1988, 3(2):57-62. (in Chinese)
[15] WU F, HUANG J, XU M, FOX E G P, BEATTIE G A C, HOLFORD P, CEN Y, DENG X. Host and environmental factors influencing ‘Candidatus Liberibacter asiaticus’ acquisition in Diaphorina citri. Pest Management Science, 2018, 74(12):2738-2746.
doi: 10.1002/ps.2018.74.issue-12
[16] INOUE H, OHNISHI J, ITO T, TOMIMURA K, MIYATA S, IWANAMI T, ASHIHARA W. Enhanced proliferation and efficient transmission of ‘Candidatus Liberibacter asiaticus’ by adult Diaphorina citri after acquisition feeding in the nymphal stage. Annals of Applied Biology, 2009, 155(1):29-36.
doi: 10.1111/aab.2009.155.issue-1
[17] PELZ-STELINSKI K S, BRLANSKY R H, EBERT T A, ROGERS M E. Transmission parameters for Candidatus Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). Journal of Economic Entomology, 2010, 103(5):1531-1541.
doi: 10.1603/EC10123
[18] HALL D G, ALBRECHT U, BOWMAN K D. Transmission rates of ‘Ca. Liberibacter asiaticus’ by Asian citrus psyllid are enhanced by the presence and developmental stage of citrus flush. Journal of Economic Entomology, 2016, 109(2):558-563.
doi: 10.1093/jee/tow009
[19] 陈循渊, 廖长青. 柑桔木虱生物学特性观察及其与黄龙病的关系. 中国柑桔, 1982(4):14-17.
CHEN X Y, LIAO C Q. Observation on biological characteristics of Diaphorina citri and its relationship with citrus Huanglongbing. Chinese Citrus, 1982(4):14-17. (in Chinese)
[20] LEE J A, HALBERT S E, DAWSON W O, ROBERTSON C J, KEESLING J E, SINGER B H. Asymptomatic spread of Huanglongbing and implications for disease control. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(24):7605-7610.
[21] GOTTWALD T R. Current epidemiological understanding of citrus Huanglongbing. Annual Review of Phytopathology, 2010, 48:119-139.
doi: 10.1146/phyto.2010.48.issue-1
[22] LI W, HARTUNG J S, LEVY L. Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus Huanglongbing. Journal of Microbiological Methods, 2006, 66(1):104-115.
doi: 10.1016/j.mimet.2005.10.018
[23] KIM J S, SAGARAM U S, BURNS J K, LI J L, WANG N. Response of sweet orange (Citrus sinensis) to ‘Candidatus Liberibacter asiaticus’ infection: Microscopy and microarray analyses. Phytopathology, 2009, 99(1):50-57.
doi: 10.1094/PHYTO-99-1-0050
[24] BAO M, ZHENG Z, SUN X, CHEN J, DENG X. Enhancing PCR capacity to detect ‘Candidatus Liberibacter asiaticus’ utilizing whole genome sequence information. Plant Disease, 2020, 104(2):527-532.
doi: 10.1094/PDIS-05-19-0931-RE
[25] SPURR A R. A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research, 1969, 26(1/2):31-43.
doi: 10.1016/S0022-5320(69)90033-1
[26] WANG Z, YIN Y, HU H, YUAN Q, PENG G, XIA Y. Development and application of molecular-based diagnosis for ‘Candidatus Liberibacter asiaticus’, the causal pathogen of citrus Huanglongbing. Plant Pathology, 2006, 55(5):630-638.
doi: 10.1111/ppa.2006.55.issue-5
[27] FU S, BAI Z, SU H, LIU J, HARTUNG J S, ZHOU C, WANG X. Occurrence of prophage and historical perspectives associated with the dissemination of Huanglongbing in mainland China. Plant Pathology, 2020, 69(1):132-138.
doi: 10.1111/ppa.v69.1
[28] WU F, JIANG H, BEATTIE G A, HOLFORD P, CHEN J, WALLIS C M, ZHENG Z, DENG X, CEN Y. Population diversity of Diaphorina citri (Hemiptera: Liviidae) in China based on whole mitochondrial genome sequences. Pest Management Science, 2018, 74(11):2569-2577.
doi: 10.1002/ps.2018.74.issue-11
[29] 谢佩华, 苏朝安, 林自国. 柑桔木虱生物学研究. 浙江农业大学学报, 1989, 15(2):198-202.
XIE P H, SU C A, LIN Z G. Studies on the biology of the citrus psylla, Diaphorina citri Kuwayama (Homoptera, Psyllidae). Acta Agriculturae Universitatis Zhejiangensis, 1989, 15(2):198-202. (in Chinese)
[30] JAIN M, MUNOZ-BODNAR A, ZHANG S, GABRIEL D W. A secreted ‘Candidatus Liberibacter asiaticus’ peroxiredoxin simultaneously suppresses both localized and systemic innate immune responses in planta. Molecular Plant-Microbe Interactions, 2018, 31(12):1312-1322.
doi: 10.1094/MPMI-03-18-0068-R
[31] PANDEY S S, WANG N. Targeted early detection of citrus Huanglongbing causal agent ‘Candidatus Liberibacter asiaticus’ before symptom expression. Phytopathology, 2019, 109(6):952-959.
doi: 10.1094/PHYTO-11-18-0432-R
[32] PAUL M J, FOYER C H. Sink regulation of photosynthesis. Journal of Experimental Botany, 2001, 52(360):1383-1400.
doi: 10.1093/jexbot/52.360.1383
[33] 刘登全, 崔朝宇, 蒋军喜, 龙珑. 不同柑橘品种对黄龙病的抗性鉴定. 江西农业大学学报, 2014, 36(1):97-101.
LIU D Q, CUI C Y, JIANG J X, LONG L. Resistance identification of difference citrus cultivars against Huanglongbing. Acta Agriculturae Universitatis Jiangxiensis, 2014, 36(1):97-101. (in Chinese)
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