Agricultural Sciences in China

2008, 7(11): 1348-1354

November 2008

Comparative Analysis of Population Genetic Structure in Bemisia tabaci (Gennadius) Biotypes B and Q Based on ISSR Marker
CHU Dong1, 2, WAN Fang-hao3, XU Bao-yun2, WU Qing-jun2 and ZHANG You-jun2
1 2 3

High-Tech Research Center, Shandong Academy of Agricultural Sciences, Jinan 250100, P.R.China Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China The State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China

Abstract
Bemisia tabaci (Gennadius) biotypes B and Q are two invasive biotypes in the species complex. The comparison of the population genetic structure of the two biotypes is of significance to show their invasive mechanism and to their control. The intersimple sequence repeats (ISSR) marker was used to analyze the 16 B-biotype populations and 4 Q-biotype populations worldwide with a Trialeurodes vaporariorum population in Shanxi Province, China, and a B. tabaci non-B/Qbiotype population in Zhejiang Province, China, was used as control populations. The analysis of genetic diversity showed that the diversity indexes of biotype Q including Neis gene diversity index, Shannon informative index, and the percentage of polymorphic loci were higher than those of biotype B. The high genetic diversity of biotype Q might provide the genetic basis for the excellent ecological adaptation. Cluster analysis suggested that the ISSR could not be used in the phylogenetic analysis though it could easily distinguish the biotypes of B. tabaci. The difference of the population genetic structure between the biotype B and the biotype Q exists based on the ISSR marker. Meanwhile, the results suggested that the molecular marker has its limitation in the phylogenetic analysis among the biotypes of B. tabaci. Key words: invasive mechanism, Bemisia tabaci biotype B, Bemisia tabaci biotype Q, genetic structure, ISSR

INTRODUCTION
Bemisia tabaci (Gennadius) is an important agricultural pest worldwide, which can not only directly damage the plants, but also transmit numerous plant viruses (Jones 2003). The whitefly is generally considered to be species complex, which includes several genetically differentiated populations. Some populations have been labeled as different biotypes, among them the biotype B and the biotype Q are the two most invasive biotypes. B. tabaci biotype B had been an invasive pest worldwide since its outbreak in the USA during the middle-

late 1980s. B. tabaci biotype Q originated from Mediterranean regions has successfully introduced into nonMediterranean countries including China (Chu et al. 2005), the USA, Guatemala, Mexico, and Japan (Ueda and Brow 2006), and has caused damages during the recent years. The main biotype of the whitefly has caused severe damages in most regions of China (Zhang 2000; Liu et al. 2005), and was identified as biotype B based on the mitochondrial cytochrome oxidase I (mtDNA COI). Meanwhile, the biotype Q has invaded into Yunnan, Beijing, Henan (Chu et al. 2006), Zhejiang (Xu et al. 2006), and Taiwan (Hsieh et al. 2007) of China. The comparative analysis of population genetic

This paper is translated from its Chinese version in Scientia Agricultura Sinica. CHU Dong, Ph D, E-mail: chudong1977@hotmial.com; Correspondence ZHANG You-jun, Tel: +86-10-82109518, E-mail: zhangyj@mail.caas.net.cn

2008, CAAS. All rights reserved. Published by Elsevier Ltd.

Comparative Analysis of Population Genetic Structure in Bemisia tabaci (Gennadius) Biotypes B and Q Based

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structure of the two biotypes will provide significant results to show the genetic mechanism of invasion and also guide in the management of these biotypes (Suarez et al. 1999; Tsutsui et al. 2001). The study will also show the rapid evolutional process and its influential factors of alien species (Chu et al. 2004). Chu et al. (2007a) have studied the genetic structure of the two biotypes using the random amplified polymorphic DNA (RAPD). The intersimple sequence repeat (ISSR) marker is from the RAPD, except the primer used is ISSR. Compared with the RAPD primers, the ISSR primers has the stability of DNA fingerprinting pattern and the efficiency of the RAPD and is easy to operate (An et al. 2002). During the recent years, it has been widely used in the study of invasive alien species (Chu et al. 2007b; Gui et al. 2007; Wang et al. 2007). The analysis of biotype A and biotype B based on ISSR by Perring et al. (1993) showed that the genetic similarity of them is only about 10%. The study on the genetic structure of biotype B and biotype Q based on ISSR has not been carried out until now. In the present study, the genetic structure of biotype B and biotype Q was analyzed using ISSR marker to further show the characteristics of the genetic structure of the two biotypes. The research will be helpful to recognize the genetic basis of the invasive biotype of B. tabaci. The result was also compared with those based on RAPD and mt
Table 1 Data of whitefly samples collected from different locations
Population code 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 - indicates unknown. Whitefly species and B. tabaci biotype B. tabaci biotype B B. tabaci biotype B T. vaporariorum B. tabaci biotype B B. tabaci biotype Q B. tabaci biotype B B. tabaci biotype Q B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci non-B/Q biotype B. tabaci biotype Q B. tabaci biotype B B. tabaci biotype Q B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B B. tabaci biotype B

COI markers (Chu et al. 2006, 2007a). The characteristics and limitation of the ISSR were discussed in the biotype identification and phylogenetic analysis.

MATERIALS AND METHODS

Whiteflies
Whiteflies were collected from 22 places throughout the world. The sites, hosts, species/biotypes, time of collection, and acronym were explained in Table 1. All samples were stored at -20C. Biotype of B. tabaci was determined based on mt COI. The biotype Q populations from Haidian of Beijing, and Kunming of Yunnan are invasive populations (Chu et al. 2006). Biotype B from Arizona, Texas, California, and Israel, and biotype Q from Israel were used as control populations. Dr. Judy Brown from Arizona University and Dr. Matthew Ciomperlic from the United States Department of Agriculture provided B. tabaci biotype B from Arizona and Texas, respectively. B. tabaci from Israel was provided by Dr. Rami Horowitz of Israel Volcani Agricultural Research Center.

DNA extraction of different populations

The DNA extraction method proposed by Chu et al.

Sampling location Zhengzhou, Henan Beijing Yuncheng, Shanxi Israel Israel Spain Spain Arizona, USA California, USA Australia Beijing Zaozhuang, Shandong Nanjing, Jiangsu Hangzhou, Zhejiang Hangzhou, Zhejiang Kunming, Yunnan Tulufan, Xinjiang Beijing Taian, Shandong Zhengzhou, Henan Zhengzhou, Henan Zhengzhou, Henan

Host plant Broccoli Cucumber Cotton Cotton Cotton Hibiscus Eggplant Pepper Cucumber Cotton Poinsettia Poinsettia Cucumber Cotton Cabbage Pumpkin

Sampling date 2003.10 2003.8 2003.7 2003.8 2003.8 2003.8 2003.8 2003.8 2003.9 2004.1 2003.8 2003.8 2003.7 2003.8 2003.8 2003.8 2003.10 2003.10 2003.8 2003.12 2003.12 2003.10

Acronym HeN1-B BeiJ1-B ShanX-TV Israel1-B Israel2-Q Spain-B Spain-Q AZ-B CL-B Aus-B BeiJ2-B ShanD1-B JiangS-B ZheJ-B ZheJ-NBQ YunN-Q XinJ-B BeiJ3-Q ShanD2-B HeN2-B HeN3-B HeN4-B

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CHU Dong et al.

was followed (Chu et al. 2007a). A total of 10 adult individual whiteflies were ground in 100 L lysis buffer (1% SDS, 10 mmol L-1 Tris-HCl, pH = 8.0, 25 mmol L-1 NaCl, 25 mmol L-1 EDTA) in the 0.2 mL Eppendorf tube.

Reaction system and conditions

The six primers used were (GACAC) 3, (GACA) 4 , (TCC) 5, (AGG)5, (ACTG)4 (Perring et al. 1993) and (5-AGAGGTGGGCAGGTG-3) (Gong et al. 2001). Polymerase chain reaction (PCR) was carried out in the MJ-100 PCR machine, and the reaction conditions were same as described by Perring et al. (1993). The PCR was performed under following conditions: denaturation at 94C for 5 min, followed by 35 cycles (94C for 1 min, 52C for 1 min, 72C for 2 min), and a final extension at 72C for 5 min. The products were stored at 4C.

were put into the software POPGEN32 to calculate the genetic distance (Nei 1972), the Neis gene diversity index (Nei 1973), Shannon informative index (Lewontin 1972) and percentage of polymorphic loci of different populations of B. tabaci. Meanwhile, the cluster analysis was performed in the DPS2000 (ver. 3.1.0.1) (Tang and Feng 1997) using 0-1 systemic cluster (Jaccard distance/UPGMA method) based on the statistical data.

RESULTS
Detection results
The results showed that the ISSR using six primers could all result in the polymorphic pattern (Figs.1 and 2). The result of Trialeurodes vaporariorum (code 3 in the Figs.1 and 2) was obviously different from these of B. tabaci.

Data analysis
The products were separated on the 1.5% agarose gels in 0.5 TBE buffer at 80 V. The data obtained

Diversity index
The genetic diversity analysis of different populations

Fig. 1 Example of ISSR patterns generated with primer (AGG) 5. Population codes as shown in Table 1. M, 100-bp DNA ladder.

Fig. 2 Example of ISSR patterns generated with primer (5-AGAGGTGGGCAGGTG-3). Population codes as shown in Table 1. M, 100bp DNA ladder.

2008, CAAS. All rights reserved. Published by Elsevier Ltd.

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of B. tabaci biotypes (Table 2) showed the diversity indexes of biotype Q including Neis gene diversity index, Shannon informative index, and percentage of polymorphic loci (0.1764, 0.2544, 41.10, respectively) were higher than those of biotype B (0.0991, 0.1577, 38.36, respectively).

to 0.4838 and Zhejiang non-B/Q biotype and biotype B from 0.4403 to 0.6016. The ISSR could distinguish different biotypes of B. tabaci based on the cluster analysis (Fig.3).

DISCUSSION
Genetic diversity of biotypes B and Q based on ISSR analysis
The result on the genetic structure of biotype B and biotype Q analyzed using ISSR (Table 2) showed diversity indexes of biotype Q including Neis gene diversity index, Shannon informative index, and percentage of polymorphic loci were higher than those of biotype B. This result is similar with the analysis based on

Genetic distance and cluster

The data in Table 3 showed the genetic distance between the T. vaporariorum and B. tabaci ranged from 0.5528 to 0.8565. The genetic distance of total biotype B ranged from 0.0420 to 0.2474 and total biotype Q from 0.1961 to 0.3586. The genetic distance between the biotype Q and biotype B ranged from 0.5063 to 0.8565. The distances between the Zhejiang non-B/Q biotype and biotype Q ranged from 0.4403

Table 2 Genetic diversity of Bemisia tabaci biotype-B and biotype-Q populations and all Bemisia tabaci populations
Populations 1) Biotype B (16) Biotype Q (4) Total B. tabaci biotypes
1)

Neis gene diversity index 0.0991 0.1764 0.2398

Shannon informative index 0.1577 0.2544 0.3808

Percentage of polymorphic loci 38.36 41.10 89.04

The number in the parenthesis indicates the number of populations analyzed.

Fig. 3 Dendrogram for different Bemisia tabaci biotypes with Trialeurodes vaporariorum as outgroup acronyms as shown in Table 1.

RAPD (Chu et al. 2007a; Moya et al. 2001). It is generally considered that the genetic diversity is closely related to the adaptability to the environment and potential evolution. Both biotype Q and biotype B are invasive biotypes of B. tabaci, which have introduced into many countries whereas there is a certain difference between the two biotypes. Some of the published data showed that the biotype Q is better than the biotype B in some biological characteristics, for example, biotype Q has better biological advantages on some plant hosts (Muniz 2000; Muniz and Nombela 2001; Nombela et al. 2001), has similar or stronger ability to transmit viruses (Berdiales et al. 1999; Parrella et al. 2004), and has higher and more steady resistance to some chemical pesticides than biotype B (Nauen et al. 2002; Elbert and Nauen 2000; Dennehy et al. 2005). The high genetic diversity of biotype Q might provide the genetic basis for biological variance and ecological adaptation. Although the genetic diversity of alien species might be influenced by all kinds of factors during the invasion, can the influence result in the biological changes of

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The results showed that the ISSR using six primers could all result in the polymorphic pattern (Figs.1 and 2). They can be used to distinguish T. vaporariorum and B. tabaci easily. The indexes of genetic diversity of biotype B or biotype Q based on ISSR are higher than those of them based on RAPD (Chu et al. 2007a; Moya et al. 2001). Thus, the percentage of polymorphic loci of different biotypes based on ISSR is higher than based on RAPD. The ISSR could distinguish different biotypes of B. tabaci based on the genetic distance (Table 3) and cluster analysis (Fig.3). But, this marker could be used to analyze the phylogenetic relationship between different biotypes of B. tabaci like RAPD (Chu et al. 2007a) marker. First, the genetic distance between some biotypes was even higher than that between the T. vaporariorum and two biotypes of B. tabaci. Secondly, the biotype Q from Israel has differentiation with the biotype Q from Yunnan, Beijing, and Spain based on phylogenetic analysis using the mt COI sequences (Chu et al. 2006). The relationship does not appear in the cluster based on ISSR (Fig.3). These results suggest that ISSR might have its limitation in the phylogenetic analysis among different biotypes of B. tabaci.

CONCLUSION

Genetic distance and phylogenetic analysis of biotypes B and Q

alien species and become invasive alien species? The intensive research on the problem will be significant to show the genetic mechanism of the new harmful biotype.

Table 3 The genetic distance between the populations of different biotypes of Bemisia tabaci1)
7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

Population code 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
**** **** **** **** ****

The result on the genetic structure of biotype B and biotype Q based on ISSR showed that they were different in the genetic structure. The indexes of genetic diversity of biotype Q were higher than those of biotype B. The high genetic diversity of biotype Q might provide the genetic basis for the excellent ecological adaptation. The results suggested that the ISSR marker has its limitation in the phylogenetic analysis among the biotypes though it could be used to distinguish the biotypes of B. tabaci.
0.9452 0.9041 0.5068 0.9041 0.4658 0.8630 0.6027 0.8767 0.8630 0.5205 0.8904 0.4795 0.8219 0.5616 0.8767 0.9178 0.8767 0.4795 0.8767 0.4384 0.8356 0.6027 0.9452 0.8767 0.8767 0.8904 0.4658 0.8904 0.4247 0.8493 0.5890 0.9041 0.8630 0.9589
***

****

0.9041

****

0.5068 0.5753

****

0.9041 0.9178 0.4932

****

0.4932 0.4521 0.5479 0.4521

****

0.8630 0.8493 0.5342 0.8767 0.4932

****

0.5753 0.5068 0.4658 0.5342 0.7808 0.4932

0.9452 0.9041 0.4795 0.9041 0.4932 0.8356 0.5479 0.8904 0.8493 0.8630 0.8767
****

0.9863 0.9178 0.5205 0.8904 0.4795 0.8493 0.5616 0.9315 0.8630 0.9041 0.8630 0.9315
****

0.9589 0.8630 0.4932 0.8630 0.4795 0.8219 0.5616 0.9315 0.8630 0.9315 0.8904 0.9041 0.9452

0.6027 0.6164 0.5479 0.6164 0.6164 0.6301 0.6438 0.6027 0.6438 0.6027 0.5890 0.6027 0.5890 0.5616
****

0.5068 0.4658 0.5342 0.4658 0.8219 0.5342 0.7123 0.4795 0.4932 0.4795 0.4384 0.4795 0.4932 0.4932 0.6301
****

0.9315 0.8630 0.4658 0.8904 0.4795 0.8219 0.5890 0.9315 0.8356 0.9315 0.8904 0.9041 0.9178 0.9452 0.6164 0.4932
****

0.5479 0.4795 0.4932 0.5068 0.6986 0.5753 0.7808 0.5753 0.5616 0.5753 0.5616 0.5479 0.5342 0.5616 0.6438 0.7945 0.5616
****

0.9589 0.8630 0.4658 0.8904 0.4521 0.8493 0.5890 0.9589 0.8630 0.9315 0.8904 0.9315 0.9452 0.9452 0.5890 0.4658 0.9452 0.5890
****

0.8904 0.8219 0.4247 0.8493 0.4384 0.7808 0.5753 0.8904 0.7945 0.9178 0.8767 0.8904 0.8767 0.9041 0.5479 0.4521 0.9315 0.5479 0.9315
****

0.9315 0.8904 0.5205 0.8904 0.5342 0.8219 0.5616 0.9041 0.8630 0.8767 0.8356 0.9315 0.9178 0.9178 0.5890 0.5205 0.8904 0.5616 0.9178 0.9041 0.1316 0.1473 0.1633 0.1473 0.1473 0.4403 0.7069 0.1796 0.5769 0.1473 0.2300 0.1473 0.1473 0.0420 0.1473 0.1008 0.0710 0.5063 0.7351 0.0710 0.5528 0.0710 0.0858 0.1316 0.0710 0.1316 0.1473 0.1161 0.5293 0.8247 0.1161 0.5769 0.1161 0.1316 0.1796 0.1161 0.0710 0.1008 0.5063 0.7351 0.1008 0.6016 0.0710 0.1161 0.0710 0.1008 0.0564 0.5293 0.7069 0.0858 0.6269 0.0564 0.1316 0.0858 0.0858 0.5769 0.7069 0.0564 0.5769 0.0564 0.1008 0.0858 0.0278 0.4618 0.4838 0.4403 0.5293 0.6016 0.5293 0.5769 0.7069 0.2300 0.7641 0.7940 0.6529 0.7641 0.5769 0.0564 0.0710 0.1161 0.0564 0.5293 0.6016 0.5769 0.5293 0.0710 0.0858 0.0278
**** 0.1008 0.0710 0.0858

0.9315 0.8356 0.4658 0.8630 0.4521 0.8219 0.5616 0.9315 0.8630 0.9315 0.8904 0.9041 0.9178 0.9726 0.5616 0.4658 0.9452 0.5890 0.9726 0.9315 0.9178
****

0.1008 0.6795 0.1008 0.7069 0.1473 0.5528 0.0564 0.1316 0.0858 0.1316 0.0564 0.0138 0.0420 0.5063 0.6795 0.0710 0.6016 0.0420 0.1161 0.0710 0.0710 0.1316 0.0564 0.1008 0.1161 0.0710 0.0710 0.5063 0.7351 0.0710 0.5528 0.0420 0.1161 0.1008 0.0710

0.5528 0.0858 0.7940 0.1633 0.6795 0.1008 0.1473 0.1316 0.1161 0.1008 0.0858 0.1473 0.4838 0.7641 0.1473 0.7351 0.1473 0.1961 0.1161 0.1796

0.7069 0.6016 0.6269 0.7641 0.6795 0.6529 0.7351 0.7641 0.7351 0.6529 0.7069 0.6016 0.6269 0.7641 0.7069 0.7641 0.8565 0.6529 0.7641

0.7940 0.1316 0.6269 0.1008 0.1161 0.1316 0.1161 0.1008 0.1161 0.1473 0.4838 0.7641 0.1161 0.6795 0.1161 0.1633 0.1161 0.1473

0.7069 0.2474 0.7641 0.7351 0.8247 0.8565 0.7069 0.7351 0.7351 0.4838 0.1961 0.7351 0.3586 0.7940 0.8247 0.6269 0.7940

2008, CAAS. All rights reserved. Published by Elsevier Ltd.

0.7069 0.1473 0.1961 0.1796 0.1633 0.1796 0.1633 0.1961 0.4618 0.6269 0.1961 0.5528 0.1633 0.2474 0.1961 0.1961

0.5063 0.5769 0.5063 0.5293 0.6016 0.5769 0.5769 0.4403 0.3392 0.5293 0.2474 0.5293 0.5528 0.5769 0.5769

CHU Dong et al.

1)

Outgroup: Trialeurode vaporariorum; the codes as shown in Table 1. Neis genetic identity (above diagonal) and genetic distance (below diagonal).

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1353

Acknowledgements
This work was funded by the National Program on Basic Research Projects of China (973 Program, 2002CB111400), National Natural Science Foundation of China (30500331, 30771410), the Natural Science Foundation of Beijing Municipal (6062024), Excellent Young Scientist Foundation of Shandong Province (2007BS06013), Innovation Foundation of Shandong Academy of Agricultural Sciences (Q2006B05; 2007YCX030), and the National Key Technologies R&D Program of China during the 11th Five-Year Plan period (2006BAD08A18). We are grateful to Dr. Judy Brown of Arizona University, Dr. Matthew Ciomperlic of United States Department of Agriculture, Dr. Rami Horowitz of Israel Volcani Agricultural Research Center for providing whiteflies.

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