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"

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