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Original Article

Genetic Diversity of Plasmodium vivax in Clinical Isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3α, PvMSP3β) Genes and Eight Microsatellite Markers

Supinya Thanapongpichat1,*, Thunchanok Khammanee2, Nongyao Sawangjaroen2, Hansuk Buncherd1, Aung Win Tun3
The Korean Journal of Parasitology 2019;57(5):469-479.
Published online: October 31, 2019

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*Corresponding author: (supinya.th@psu.ac.th)
• Received: April 18, 2019   • Revised: September 19, 2019   • Accepted: September 21, 2019

Copyright © 2019 by The Korean Society for Parasitology and Tropical Medicine

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Genetic Diversity of Plasmodium vivax in Clinical Isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3α, PvMSP3β) Genes and Eight Microsatellite Markers
Korean J Parasitol. 2019;57(5):469-479.   Published online October 31, 2019
DOI: https://doi.org/10.3347/kjp.2019.57.5.469
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Genetic Diversity of Plasmodium vivax in Clinical Isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3α, PvMSP3β) Genes and Eight Microsatellite Markers
Korean J Parasitol. 2019;57(5):469-479.   Published online October 31, 2019
DOI: https://doi.org/10.3347/kjp.2019.57.5.469
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Genetic Diversity of Plasmodium vivax in Clinical Isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3α, PvMSP3β) Genes and Eight Microsatellite Markers
Image Image Image
Fig. 1 Map of the study sites in Southern Thailand.
Fig. 2 Restriction fragment length polymorphism patterns of Plasmodium vivax. (A) PvMSP3α after PCR/RFLP using HhaI enzyme. (B) PvMSP3β after PCR/RFLP using PstI enzyme. (C) PvMSP1 F2 after PCR/RFLP using AluI enzyme. M represented 100-bp marker.
Fig. 3 Frequency distribution of the number of loci with mixed-clone infections isolated from Southern Thailand. Fifty-seven multiple-clone infections were detected for Chumphon, Ranong, Surat Thani and Phang Nga provinces, respectively.

Fig. 1

Fig. 2

Fig. 3

Genetic Diversity of Plasmodium vivax in Clinical Isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3α, PvMSP3β) Genes and Eight Microsatellite Markers

Primer sequences for Plasmodium vivax genotyping

Gene Primer Sequence (5′→3′) Reference
Merozoite surface protein gene markers
PvMSP3α (N1) 3α-OF CAGCAGACACCATTTAAGG Bruce et al., 1999 [23]
3α-OR CCGTTTGTTGATTAGTTGC
PvMSP3α (N2) 3α-NF GACCAGTGTGATACCATTAAC
3α-NR ATACTGGTTCTTCGTCTTCAGG
PvMSP3β (N1) 3β-OF GGTATTCTTCGCAACACTC Yang et al., 2006 [16]
3β-OR GCTTCTGATGTTATTTCCAG
PvMSP3β (N2) 3β-NF CGAGGGGCGAAATTGTAAACC
3β-NR GCTGCTTCTTTTGCAAAGG
PvMSP1 F2 (N1) VM1-O2F GATGGAAAGCAACCGAAGAAGGGAAT Imwong et al., 2005 [13]
VM1-O2R AGCTTGTACTTTCCATAGTGGTCCAG
PvMSP1 F2 (N2) VM1-N2F AAAATCGAGAGCATGATCGCCACTGAGAAG
Microsatellite markers
Pv1.501 Forward TCCTGTAACTCCTGCTCTGT Imwong et al., 2007 [18]
motif: GGTGAGA Reverse CTTACTTCTACGTGCCCACT
Forward, s-n 6FAM-AATTGTAGTTCAGCCCATTG
Pv3.27 Forward AAGCTGCACTGAATTATGCT
motif: AAAC Reverse TTCCAAATGTATGTGCAGTC
Forward, s-n 6FAM-AGCACAAGCATATGCAAAA
Pv3.502 Forward CCATGGACAACGGGTTAG
motif: AACGGATG Reverse TCCTACTCAGGGGGAATACT
Forward, s-n HEX-GTGGACCGATGGACCTAT
Pv6.34 Forward CAAATCATGGTAGCCTCCTA
motif: AC Reverse GCTATGCATGTGTGGATGT
Forward, s-n 6FAM-TTAAGCTTCTGCATGCTCTT
Pv8.504 Forward AAAAGACTAGGCAGTTGACG
motif: TGACCAA Reverse AGTGTGTGTAGTGGGTGGAG
Forward, s-n HEX-TCTTCTCGTTCTCCTTTTCTG
Pv14.297 Forward TGACATCTTTCAAATATTCCTTT
motif: AAG Reverse TGAAAAATGTTCCGCTACTT
Forward, s-n HEX-TACACCCTTTAGGTCCTCGT
Pv11.162 Forward GTAGGAACACGCCACGTT
motif: ATAC Reverse TAAATGACACTTTGGCTTCC
Forward, s-n HEX-TTTGTTAGGAGATCCGTCTG
MS1 Forward 6-FAM TCAACTGTTGGAAGGGCAAT Karunaweera et al., 2007 [24]
motif: GAA Reverse ctgtcttTTGCTGCGTTTTTGTTTCTG

N1=Nest 1 (Primary) reaction; N2=Nest 2 (Secondary) PCR reaction.

s-n, seminested.

Frequencies of each allelic fragment pattern of PvMSP3α gene in 62 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with HhaI restriction enzyme

Genotype (kb) Allele type HhaI restriction fragments (bp) No. of samples of each Province Total No. of samples Frequency (%)
Chumphon Phang Nga Ranong Surat Thani
A (~1.9) A1 1,000+500+300 2 0 0 0 2 3.23
A2 1,000+500+400 0 0 2 0 2 3.23
A3 1,000+500+280+210 1 0 9 0 10 16.13
A4 1,000+450+280+210 1 1 7 0 9 14.53
A5 1,000+400+280+210 5 0 3 0 8 12.9
A6 1,000+350+280+210 2 1 3 1 6 9.68
A7 1,000+300+280+200 0 0 3 0 4 6.45
A8 1,000+300+250+150 1 2 2 0 5 8.06
A9* 1,000+450+400+250+200 0 0 1 0 1 1.61
A10* 1,000+550+480+280+200 0 0 1 0 1 1.61
A11* 1,000+400+280+210+150 1 0 0 0 1 1.61
B (~1.5) B1 1,000+500 0 0 1 0 1 1.61
B2 1,000+500 0 0 1 0 1 1.61
C (~1.1) C1 1,000+200 8 1 2 0 11 17.74
Total 21 5 35 1 62 100

*Mixed genotype.

Frequencies of each allelic fragment pattern of PvMSP3β gene in 55 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with PstI restriction enzyme

Genotype (kb) Allele type PstI restriction fragment (bp) No. of samples of each Province Total No. of sample Frequency (%)
Chumphon Phang Nga Ranong Surat Thani
A (~1.7–2.2) A1 900+800+350 4 0 5 0 9 16.36
A2 1,000+850 2 0 3 0 5 9.09
A3 1,200+650 4 0 1 1 6 10.91
A4 700+600+550 1 0 2 0 3 5.45
A5 900+800 0 0 1 0 1 1.82
A6 1,200+980 0 1 0 0 1 1.82
A7 900+400+300+250 0 0 1 0 1 1.82
A8 900+700+400 0 0 1 0 1 1.82
A9* 900+800+400+300+250 0 0 4 0 4 7.27
A10* 1,500+900+800+600+400+350+250 0 0 1 0 1 1.82
A11* 900+850+350+150 0 0 3 0 3 5.45
A12* 900+600+400+300+250 1 0 1 0 2 3.64
A13* 1,200+600+500+380+200 0 1 0 0 1 1.82
A14* 1,200+900+800+600+300 0 1 1 0 2 3.64
B (~1.4–1.5) B1 1,500 2 0 4 0 6 10.91
B2 1,200+300 0 0 1 0 1 1.82
B3 900+400+200 0 0 1 0 1 1.82
B4 600+400+300+200 0 0 1 0 1 1.82
B5 900+600+400+250 0 0 3 0 3 5.45
B6* 900+700+400 3 0 0 0 3 5.45
Total 17 3 34 1 55 100

*Mixed genotype.

Frequencies of each allelic fragment pattern of PvMSP1 F2 gene in 67 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with AluI restriction enzyme

Genotype (kb) Allele type AluI restriction fragment (bp) No. of samples of each Province Total No. of sample Frequency (%)
Chumphon Phang Nga Ranong Surat Thani
A Aa 170+230+320+450 1 0 0 0 1 1.49
Ab 140+170+280+450 1 0 2 4 7 10.45
Ac 140+170+230+280 1 0 1 0 2 2.99
Ad 170+320+500 2 0 0 0 2 2.99
1,150 pb Ae 140+320+480 0 0 4 0 4 5.97
Af 170+320+480 3 0 0 2 5 7.45
Ag 170+280+480 0 1 0 1 2 2.99
Ah 140+280+480 3 1 5 0 9 13.42
Ai 140+230+280 7 0 3 0 10 14.92
Aj 140+170+280 0 0 1 0 1 1.49
B Ba 170+380+500 1 0 2 0 3 4.48
Bb 170+230+500 0 0 2 0 2 2.99
Bc 140+230+500 0 0 3 1 4 5.97
1,090 pb Bd 140+280+380 4 0 0 0 4 5.97
Be 140+230+320 1 0 1 0 2 2.99
Bf 170+230+280 0 0 2 1 3 4.48
Bg 140+210+240 5 0 1 0 6 8.96
Total 29 2 27 9 67 100

All microsatellite fragment sizes and allele frequency of Plasmodium vivax isolates from Southern Thailand

Marker (size, bp) Microsatellite analysis
Pv1.501 (76–195) Pv 3.27 (85–240) Pv 3.502 (128–265) Pv 6.34 (136–200) Pv 8.504 (191–317) Pv 11.162 (172–228) Pv 14.297 (180–229) MS1 (228–246)
Samples amplified 95 100 99 97 100 94 102 47
All detected alleles 128 125 109 104 104 97 109 49
Microsatellite fragmentsa (%) 76 (0.8) 92 (12.6) 134 (2.8) 134 (1.9) 198 (9.5) 176 (1.0) 180 (6.4) 225 (12.2)
83 (5.4) 96 (3.1) 142 (4.6) 136 (1.0) 205 (10.5) 180 (70.1) 183 (2.8) 228 (36.7)
90 (10.8) 100 (5.5) 150 (27.5) 138 (3.8) 212 (21.9) 184 (16.5) 186 (9.2) 231 (22.4)
97 (16.2) 104 (7.9) 158 (8.3) 140 (4.8) 219 (26.7) 188 (4.1) 189 (12.8) 234 (10.2)
104 (14.6) 108 (5.5) 166 (15.6) 142 (22.1) 226 (6.7) 192 (3.1) 192 (22.0) 237 (2.0)
111 (13.1) 112 (7.1) 174 (9.2) 144 (6.7) 233 (8.6) 196 (5.2) 195 (35.8) 240 (16.3)
118 (6.9) 116 (6.3) 182 (3.7) 146 (11.5) 247 (2.9) 198 (10.1)
125 (3.1) 120 (4.7) 190 (0.9) 148 (12.5) 254 (3.8) 201 (0.9)
132 (7.7) 124 (1.6) 198 (12.8) 150 (3.8) 261 (1.0)
139 (4.6) 128 (3.1) 206 (7.3) 152 (10.6) 268 (2.9)
146 (4.6) 132 (8.7) 222 (1.8) 154 (5.8) 275 (2.9)
153 (4.6) 136 (7.9) 246 (5.5) 156 (4.8) 289 (2.9)
160 (1.5) 144 (2.4) 158 (4.8)
160 (1.5) 148 (0.8) 160 (1.0)
167 (1.5) 152 (1.6) 166 (3.8)
181 (1.5) 156 (2.4) 198 (1.0)
188 (1.5) 160 (3.1)
164 (2.4)
176 (0.8)
188 (0.8)
204 (0.8)
208 (0.8)
212 (0.8)
236 (2.4)
240 (7.1)
No. of alleles (A) 15 24 12 16 12 6 8 5
No. of alleles per locus 1.35 1.25 1.1 1.07 1.04 1.03 1.07 1.04
HE 0.897 0.938 0.87 0.896 0.859 0.494 0.804 0.768

aAll microsatellite sizes in base pair were detected in this study which collected both predominant peaks and minor peaks.

Calculation of no. of alleles (A) and HE values were obtained from only the predominant alleles data set at each locus.

No. of alleles per locus values were calculated from all detected alleles at each locus and divided by the total number of samples amplified.

Multiple of allele sizes at eight loci from Plasmodium vivax isolates from Southern Thailand

Marker (size, bp) Microsatellite analysis
Pv1.501 (76–195) Pv 3.27 (85–240) Pv 3.502 (128–265) Pv 6.34 (136–200) Pv 8.504 (191–317) Pv 11.162 (172–228) Pv 14.297 (180–229) MS1 (228–246)
No. of multiple alleles at each locus 30 25 8 7 4 7 3 2
Multiple of allele sizes at particular locus (%) 97/132 (6.7) 96/132 (4) 150/166 (50) 140/146 (14.3) 205/212/219 (25) 186/189 (14.3) 180/188 (33.4) 227/230 (50)
97/118 (3.3) 96/104 (4) 150/166/174 (12.5) 142/150 (14.3) 205/212 (25) 189/192 (14.3) 180/196 (33.3) 227/236 (50)
90/97 (13.3) 92/132/152 (4) 150/166/198 (12.5) 142/158 (14.3) 212/219 (25) 189/195 (14.3) 180/184 (33.3)
90/118 (3.3) 92/132 (8) 166/174 (12.5) 144/148 (14.3) 212/247 (25) 192/198 (14.3)
90/111/132 (3.3) 100/156 (4) 166/198 (12.5) 146/158 (28.6) 186/195 (14.3)
90/111 (23.3) 100/108 (4) 148/154 (14.3) 180/195 (14.3)
83/76 (3.3) 104/132 (4) 183/192 (14.3)
83/104 (3.3) 108/100 (4)
167/188 (3.3) 108/112 (4)
139/160 (3.3) 108/112 (4)
132/153 (6.7) 108/188 (4)
125/146 (3.3) 112/236 (4)
125/139 (3.3) 116/120 (4)
111/132 (3.3) 116/132 (4)
111/104 (3.3) 116/144 (4)
104/125 (3.3) 116/160 (4)
104/111/132 (3.3) 116/240 (4)
104/111/118 (3.3) 120/128/132 (4)
104/111 (3.3) 124/132 (4)
160/208 (4)
132/240 (8)
236/240 (8)

The genetic diversity based on eight microsatellite markers of Plasmodium vivax isolated from four different provinces of Southern Thailand

Genetic diversity Province P-value*
Chumphon
n=38		 Phang Nga
n=4		 Ranong
n=46		 Surat Thani
n=15		 Mean
No. of alleles 9.2 2.8 9 5.4 6.6 <0.05*
HI 0.769 0.771 0.785 0.757 0.771 0.935
Multiple-clone infections, % (isolated) 58% (22/38) 50% (2/4) 48% (22/46) 73% (11/15) 57.25 0.104
MOI** 1.67 1.5 1.53 1.8 1.63 0.408

*P-value according to 1-way ANOVA,

**Multiple clone of infection.

Table 1 Primer sequences for Plasmodium vivax genotyping

N1=Nest 1 (Primary) reaction; N2=Nest 2 (Secondary) PCR reaction.

s-n, seminested.

Table 2 Frequencies of each allelic fragment pattern of PvMSP3α gene in 62 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with HhaI restriction enzyme

Mixed genotype.

Table 3 Frequencies of each allelic fragment pattern of PvMSP3β gene in 55 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with PstI restriction enzyme

Mixed genotype.

Table 4 Frequencies of each allelic fragment pattern of PvMSP1 F2 gene in 67 isolates of Plasmodium vivax from Southern Thailand as identified by PCR/RFLP after digested with AluI restriction enzyme
Table 5 All microsatellite fragment sizes and allele frequency of Plasmodium vivax isolates from Southern Thailand

All microsatellite sizes in base pair were detected in this study which collected both predominant peaks and minor peaks.

Calculation of no. of alleles (A) and HE values were obtained from only the predominant alleles data set at each locus.

No. of alleles per locus values were calculated from all detected alleles at each locus and divided by the total number of samples amplified.

Table 6 Multiple of allele sizes at eight loci from Plasmodium vivax isolates from Southern Thailand
Table 7 The genetic diversity based on eight microsatellite markers of Plasmodium vivax isolated from four different provinces of Southern Thailand

P-value according to 1-way ANOVA,

Multiple clone of infection.

Table 1

Table 2

Table 3

Table 4

Table 5

Table 6

Table 7

PHD : Parasites, Hosts and Diseases

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