DOI: https://doi.org/10.29312/remexca.v0i26.2939

Article

Bactericera cockerelli vector of Candidatus Liberibacter solanacearum, morphometrics and haplotypes in populations from Mexico

Ernesto Cerna Chávez1

Mariana Beltrán Beache2

Yisa María Ochoa Fuentes3

Omegar Hernández Bautista4

Juan Carlos Delgado Ortiz5§

1Antonio Narro Autonomous Agrarian University. Calzada Antonio Narro no. 1923, Col. Buenavista, Saltillo, Coahuila, Mexico. CP. 25315. (jabaly1@yahoo.com). 2Autonomous University of Aguascalientes-Center for Agricultural Sciences-Department of Phytotechnics. Zootechnical Post, Jesús María, Aguascalientes, Mexico. CP. 20900. (beltranmariana89@gmail.com). 3Antonio Narro Autonomous Agrarian University. Calzada Antonio Narro no. 1923. Col. Buenavista, Saltillo, Coahuila, Mexico. (yisa8a@yahoo.com). 4I+D Department, CULTA SA de CV. Boulevard Luis Echeverría Álvarez 1700, Col. Altavista, El Mante, Tamaulipas. (omegarhbautista@gmail.com). 5CONACYT-Antonio Narro Autonomous Agrarian University-Department of Agricultural Parasitology. Road Antonio Narro no. 1923, Col. Buenavista, Saltillo, Coahuila, Mexico. CP. 25315. (jdelgado@conacyt.mx).

§Corresponding author: jdelgado@conacyt.mx.

Abstract

Bactericera cockerelli is a pest of economic importance in Solanaceae in Mexico, due to the yellowings that causes in crops, as well as the transmission of Candidatus Liberibacter solanacearum. Genetic variants of this insect are described, which are related to its ability to serve as a vector. In Mexico, the distribution of B. cockerelli is very wide and information about its morphological and genetic characteristics is lacking. The objective of this research was to characterize B. cockerelli morphologically and genetically and detect the presence of Ca. L. solanacearum in populations of B. cockerelli from Solanaceae-producing areas in Mexico. For which 35 locations from 13 states were sampled, on chili, tomato, eggplant and potato crops, under different production systems. The variables body length (LC), abdomen length (LAB), and abdomen width (AAB) were measured in insects of each population, the presence of Ca. L. solanacearum was detected in the 13 sampled states, where males had the highest percentage of positive insects. The presence of Ca. L. solanacearum was not influenced by the host or production system, but by the presence of B. cockerelli.

Keywords: Ca. L. solanacearum, eggplant, haplotype, potato psyllid.

Reception date: February 2021

Acceptance date: May 2021

Introduction

Bactericera cockerelli (Hemiptera: Triozidae), also known as salerillo, pulgón saltador or psilido de la papa (potato psyllid), is a pest of economic importance in Mexico, the United States of America and New Zealand (Munyaneza, 2010). Its importance lies on the damage generated of toxin type and by the transmission of procaryotes (Ramírez et al., 2012), such  as Candidatus Liberibacter solanacearum, a pathogen of economic importance in solanaceous crops in Mexico, Honduras, Guatemala, Belize, the United States of America, New Zealand, Europe, Norway, Nicaragua, Spain, France, Sweden, Finland and Canada (Munyaneza, 2013; Hong and Civerolo, 2014; Loiseau et al., 2014; Haapalainen et al., 2018; Delgado-Ortiz et al., 2019; Henrickson et al., 2019).

Infections by Ca. L. solanacearum have caused million-dollar losses in the industry by reducing crop production and quality (Gudmestad and Secor, 2007). In addition to potato, this pathogen affects tomato, chili pepper and other species of solanaceous cultures (Liefting et al., 2009). In tomato, reductions in production have been generated by up to 60% if presented alone or up to 100% if presented together with phytoplasmas, reducing the quality of the fruit and its commercial value (Delgado-Ortiz et al., 2019). It causes an increase in the costs of crop management and vector control (Gudmestad and Secor, 2007; Greenway and Rondon, 2018).

In Mexico, the crops that have been affected by Ca. L. solanacearum are potato, chili and tomato in the states of Sinaloa, Coahuila, Michoacán and in the State of Mexico (Camacho-Tapia et al., 2011; Munyaneza et al., 2007, 2009a, 2009b; Rubio et al., 2011). Studies on genetic variability between populations of B. cockerelli from the USA have revealed the presence of two biotypes that coincide with the geographical separation of the populations analyzed, so they were called Western biotype (found in Southern California) and Central biotype (present in Colorado and Nebraska), belonging to the same species (Liu et al., 2005; Jackson et al., 2009).

The separation of biotypes into insects is attributed to the variation between populations of the same species, which may include morphological, genetic and physiological characteristics: such as the ability to survive, reproduce or cause diseases in different hostesses (Shufran and Payton, 2009). A more specific level in the classification of B. cockerelli is that of haplotypes; which has been used in order to understand the temporal and spatial population dynamics of the psyllid through genetic analysis of a single individual (Swisher et al., 2012), defining a haplotype as the genetic form that differs in any other way by variations in its DNA sequence in at least one nucleotide (Templeton, 2006), where specifically, four haplotypes of B. cockerelli have been described (Western, Central, Northwestern and Southwestern) in North and Central America (Swisher et al., 2012; 2013; 2014).

The distribution of B. cockerelli in Mexico is very wide and several specimens have been collected in various areas of agricultural importance of Durango, Tamaulipas, Mexico City, Michoacán, San Luis Potosí, Morelos, Coahuila, Chihuahua, Nayarit, Jalisco, Baja California, Guanajuato, Aguascalientes, Zacatecas and Sinaloa (Pletsch, 1947; Vega et al., 2008), without any record of its morphological and genetic characteristics.

Therefore, the objective of this research was to analyze individuals of B. cockerelli from various populations, from Solanaceae-producing areas in Mexico, to obtain their morphological and genetic characterization, as well as to detect the presence of Ca. L. solanacearum.

Materials and methods

A tour was made through the states of Aguascalientes (Ags), Zacatecas (Zac), Jalisco (Jal), Guanajuato (Gto), Hidalgo (Hgo), Puebla (Pue), San Luis Potosí (SLP), Nayarit (Nay), Nuevo León (NL), Durango (Dgo), Michoacán (Mich), Coahuila (Coah) and Tamaulipas (Tamps) from June to September 2017, collecting specimens of B. cockerelli present in Solanaceae crops, under different production systems (Table 1).

Table 1. Collection sites of B. cockerelli, host and production system.

The capture of the insects was carried out using a handheld vacuum, while in the places where the presence of adult insects was limited, foliage infested with nymphs and eggs of B. cockerelli was collected, being placed in tubes with 70% ethanol.

For the morphometric characterization of B. cockerelli, an average of 36 adults of B cockerelli collected randomly from each population were individually analyzed, to determine its external dimensions, the variables: body length (LC), abdomen length (LAB), abdomen width (AAB), wing length (LA), wing width (AA) and antenna length (LAN) were taken with the help of the Dino-Capture 2 program in a SMZ-711 stereoscopic microscope (Motic®).

Preparation of adult insects preserved in 70% ethanol consisted of placing them in a mixture of 90% glycerol to be mounted on slides exposing the parts of the insect to be measured. The data obtained were analyzed by sex and a comparison of means between the two sexes, with the program R Studio version 3.3, performing a comparison of means using a Tukey test, p≤ 0.05.

While for the determination of haplotypes of B. cockerelli, from the insects whose body was previously measured and including nymphs from some populations, DNA was extracted individually using the technique described by Doyle and Doyle (1990) modified. The haplotypes of B. cockerelli were determined using the initiators CO1 F3 (‘5-TACGCCATAC TAGCAATCGG-3’) and CO1 R3 (‘5-GAGTAACGTCGTGGTATTCC-3’) that amplify a 500 pb region of the mitochondrial gene Cytochrome C Oxidase subunit I (Swisher et al., 2012) using endpoint PCR, 4 µl of Taq&GoT Mastermix (MP Biomedicals), 0.5 µl of each first to 10 µl and 1 µl (50 ng) of DNA were used in the PCR reaction.

The reaction program was an initial denaturation of 98 °C for 30 s, followed by 30 cycles of 98 °C for 10 s, alignment at 56 °C by 20 s and extension at 72 °C by 30 s, followed by a final extension of 72 °C for 7 min, in a thermocycler Therm 1000 MaxyGeneTM, Axygen®. The generated amplicons were sequenced in both ways by Macrogene, USA, the sequences obtained were aligned with the Bio Edit programan and compared with the BLAST® program of the National Center for Biotechnological Information (NCBI).

For the detection of Candidatus Liberibacter solanacearum in B. cockerelli, the initiators Lso TX 16/23 F (5’-AATTTTAGCAAGTTCTAAGGG-3’) and Lso TX 16/23 R (5’-GGTACCTCCCATATCGC-3’) were used, which amplify a preserved region of 383pb between the 16S and 23S of the ribosomal DNA of ‘Ca. L. solanacearum’ (Ravindran et al., 2011). The PCR reaction for Lso TX 16/23 F/Lso TX 16/23 R was carried out with 4 µl of Taq&GoT Mastermix (MP Biomedicals), 0.5 µl of each initiator at 10 µl and 1 µl of DNA (50 ng), adjusting to a final reaction volume of 20 µl.

The reaction was performed under the following thermocycler conditions (Therm 1000 MaxyGeneTM, Axygen®): initial denaturation of 98 °C for 30 s; followed by 35 cycles of 98 °C by 10 s, 56 °C by 20 s for alignment and an extension of 72 °C by 30 s, followed by a final extension of 72 °C for 7 min. PCR products representative of each study population were selected to sequence in Macrogene USA to support the results obtained.

Results and discussion

For the morphometric characterization of B. cockerelli, a total of 28 populations were analyzed, from which the body dimensions of the six selected variables (LC, LAB, AAB, LA, AA, LAN) were obtained. In the analysis of variables for females (Table 2), it is highlighted that the largest records in the LC, LAB, LA, AA and AAB variables were determined in populations 2, 6 and 8, while for the LAN variable, the largest dimensions were recorded in populations 23 and 26. With the population 34, collected in Hidalgo, Tamaulipas, standing out, which recorded the smallest dimensions in the variables LC, LAB, AAB and AA, while the population 14, was the one with the lowest LA, as well as the population 20 (Moctezuma, SLP) that presented the lowest LAN.

Table 2. Morphometrics of females of B. cockerelli collected in the field.

*= populations 1, 21, 24, 25, 29, 31 and 33 were not included in the analysis as adults were not available for data collection. **= the means (mm) with the same letter within each variable show no significant difference (Tukey, p≤ 0.05).

The variables LC, LAB, AAB and LAN in females of B. cockerelli had greater separation of statistically similar groups, with variations of up to 0.5 mm between populations. The first three variables are directly related, as LAB influences the size of LC, while the variables LAB and AAB relate to the eggs load in females at the time of capture; regarding LAN, this variable responds to another stimulus, since no behavior that corresponds to the size of LC is observed, so LAN may be influenced by food availability rather than by the size of the insect, finding smaller LANs in insects with high LCs or vice versa.

For the variables LA and AA, the group separation was smaller, so it is determined as a stable size variable between the populations of females analyzed. Differences between morphometrics, biological cycle development and physiology in B. cockerelli populations, in addition to climatic and feeding factors, can also be influenced by exposure to insecticides or sex, where the largest female size and short life cycles correspond to more susceptible populations (Cerna-Chávez et al., 2018; Hardstone et al., 2010).

In the analysis of male populations (Table 3), population 34 matches the analysis of females since it records the smallest dimensions in the variables LC, LAB and LAN. While the LC variable was shown to be a more homogeneous variable, with populations 2 and 6 registering the largest dimensions in the variables LAB, AAB, LA and AA, resulting in populations 23 and 26 with the highest LAN in the males analyzed.

Table 3. Morphometrics of males of B. cockerelli collected in the field.

*populations 1, 3, 21, 24, 25, 29, 31 and 33 were not included in the analysis as adults were not available for data collection. **The means (mm) with the same letter within each variable show no significant difference (Tukey, p≤ 0.05).

In a comparison between the dimensions registered by insects of both sexes, females registered larger size for the variables analyzed Anova (F27, 658; p≤ 0.05): LC (1.870a, 1.824b); LAB (0.898a, 0.851b); AAB (0.635a, 0.532b); LA (2.509a, 2,441b); AA (0.986a, 0.949b) and LAN (0.888a, 0.895a), for females and males respectively.

In the variables analyzed the females had a larger size (±0.1 mm), with the antenna length (LAN) being the only variable where no significant difference between the sexes was observed, Vargas et al. (2013) determined that the length of the antennae is affected in the insect according to the host in which it develops, while they were unable to associate the length of the antennas with sex.

Geographic location and environmental conditions are not considered as a determinant in the body size of the populations of B. cockerelli evaluated, since within the same state there are populations in two or three of the main groups mentioned, besides that those conditions are affected by the production system under which they develop.

However, morphometrics is influenced by the host, where the highest body proportions are placed in insects fed in eggplant cultivation, while in potato, chili and tomato, no particular behavior is observed. There has been an increase in fertility, survival rate, as well as less time to complete its life cycle when B. cockerelli develops in eggplant than in pepper under laboratory conditions (Yang and Liu, 2009).

Adults of B. cockerelli are small, varying from 1.3-1.9 mm (Liu and Trumble, 2007), but this characteristic may vary depending on the host plant, the geographic origin of the populations, sex and whether the measurement was performed with field or laboratory individuals (Butler and Trumble, 2012), Vargas et al. (2013) demonstrated that the morphometrics of adults and nymphs of B. cockerelli is affected by the tomato cultivar in which it develops.

Morphometrics studies are a tool that has proved to be highly effective in analyzing the variation resulting from the physiology of individuals (variation in size), typical of population-and probably genetic (variation of form) (Jaramillo et al., 2002), the morphometric variation can be used to discriminate ‘phenotypic populations’, defined as groups with similar growth, mortality and reproduction rates (Cadrin, 2000).

In the determination of haplotypes of B. cockerelli, in all PCR products the expected amplicons of 500 bp (Figure 1) were generated, after sequencing, an identical base sequence was obtained between the samples analyzed. Following the comparison of sequences in the NCBI database, a 100% similarity was obtained with the Central haplotype (Swisher et al., 2012).

Figure 1. Amplified obtained from B. cockerelli.

Product at a weight of 500 bp with CO1 F3/CO1 R3 initiators. MP: 100 bp, band 1: population 8; band 2: population 18; band 3: population 24; band 4: population 28; band 5: population 32 and band 6: population 34; where each product represents only one individual from each population.

The Central haplotype has been found in the states of Wyoming, Nebraska, Texas and Washington in the USA; Honduras and Nicaragua in Central America; in Mexico, it has been found in the states of Toluca and Querétaro (Swisher et al., 2013). The Central haplotype of B. cockerelli differs in only one nucleotide (SNP) from the Western haplotype in residue 51 where it presents a cytosine in place of a thymine, as well as 16 SNPs from the Northwestern (Swisher et al., 2012) and two SNPs from the Southwestern haplotype (Swisher et al., 2014).

In this study, the presence of the Central haplotype is detected in the states of Aguascalientes, Jalisco, Durango, Guanajuato, Hidalgo, Puebla, Michoacán, Zacatecas, Nuevo León, Coahuila, Nayarit, San Luis Potosí and Tamaulipas. Liu et al. (2005) report two biotypes of B. cockerelli in the central and western United States of America to which Chapman et al. (2012) separated in Central and Western through high-resolution melt analysis and DNA sequencing of the mtCOI gene, these biotypes had a variation of a nucleotide at position 297 of an amplified of 421 base pairs, where the Central biotype presents a guanine (G) and Western biotype an adenine (A), declaring the Central biotype the native biotype and the Western as the invasive biotype.

According to studies conducted by Montiel et al. (2016), the Central biotype (Texas and Nebraska) and Southwestern haplotype are closely related, while the Western biotype diverges from these populations, but relates to an apparent new northwest population, which may have emerged from this biotype.

For the determination of Ca L. solanacearum in the populations of B. cockerelli, a total of 862 insects were analyzed; 348 females, 415 males and 99 nymphs (obtained from 35 populations of 13 states), of which 80.17% of females were positive to Ca. L. solanacearum, while in males the presence of the bacteria was determined in 84.57% (Table 4).

Table 4. Detection of Ca L. solanacearum in populations of B. cockerelli.

* H= females; M= males; N= nymphs.

The nymphs of B. cockerelli turned out to be excellent carriers of Ca. L. solanacearum, with 100% positive populations where adult insect capture was not possible. In all sampled states, at least one population of B. cockerelli positive for Ca. L. solanacearum was obtained, which provides a broad overview of the distribution and relationship between the vector and ‘Ca. L. solanacearum’.

In relation to the host on which the populations of B. cockerelli were collected; 92.3% of the populations from tomato resulted positive for Ca. L. solanacearum; while 83.3% of samples from chili resulted positive for the bacteria. For populations collected in potato cultivation, 100% of the samples were positive.

While the populations that resulted negative for Ca. L. solanacearum under open field production systems were population 16, 30 and 31 (Puebla and Durango, respectively) and population 5 collected in greenhouse. Thinakaran et al. (2015) have reported the preference of the Central Haplotype in the field over different hostesses, being favoritism greater in potato and tomato over pepper, eggplant and Solanaum elaeagnifolium (nightshade), where spawning is favored in potato cultivation, while under laboratory conditions the preference for eggplant over tomato cultivation and the rest of the hostesses is superior.

Cadena (1993) reported the presence of the purple tip of the potato in commercial lots of Guanajuato, Nuevo León, Coahuila, Valle de Toluca (Estado de México), Michoacán, Tlaxcala, Hidalgo and Puebla. Coinciding with the populations of  B. cockerelli positive for Ca. L. solanacearum of the states of Guanajuato, Nuevo León, Coahuila, Michoacán, Hidalgo and Puebla in this study, indicating that the disease has been present in these areas for decades, with the possibility of having dispersed to other regions and crops, which is supported by the rest of the positive populations of B. cockerelli collected in the states of Zacatecas, Aguascalientes, Jalisco, Durango, Nayarit, San Luis Potosí and Tamaulipas.

Research by Secor and Rivera (2004) documented the symptoms of the purple tip in the potato-producing region of Saltillo, Coahuila, whose etiological agent was determined by Munyaneza et al. (2007), who also related it to the presence of the vector and whose report includes the state of Nuevo León, while Rubio et al. (2011) detected Ca. L. solanacearum in the potato-producing region of Toluca, where they also found the presence of the vector. In tomato cultivation, Ca. L. solanacearum had already been reported in the states of Michoacán (Hernández, 2013) and Sinaloa (Munyaneza et al., 2009a) and chili pepper in Sinaloa, Mexico (Munyaneza et al., 2009b).

The degree of technification in crop production generally influences the incidence of pests and diseases and the severity of the attack (Jirón-Rojas et al., 2016) and according to the results of this study, it can be inferred that both the vector and the bacterium are able to adapt to any production system to which they have access. Being both vector and pathogen present in open field production lots, shade net, high tunnel and greenhouse.

The population from the town of Potrero de Vaquerías, Calvillo, Aguascalientes in open field chili cultivation, which was negative for Ca. L. solanacearum, which was found adjacent to a tomato field, whose level of infestation was considerably higher than in chili, decreasing the possibility that the captured insects carried the bacteria. The population from El Refugio, Durango, in open field chili, in number of insects obtained was limited, which decreased the probability of taking those carriers of the bacteria.

The rest of the samples negative for Ca. L. solanacearum were those from greenhouses in the towns of San Juan Tianguismanalco, Puebla and Héctor Márquez, Poanas, Durango, in chili and tomato, respectively, concluding that these populations have not been in contact with individuals or hostesses carrying the bacteria.

Conclusions

The morphometrics presented of the 28 populations of B. cockerelli analyzed represents a major advance in the characterization of this important vector in the main areas producing Solanaceae in Mexico, in addition to having determined the presence of Ca. L. solanacearum in the populations of B. cockerelli from thirteen states of Mexico. Being all the populations of B. cockerelli identified as Central haplotype.

Acknowledgements

Thanks to PhD. Julien Levy of Texas A&M University for his valuable contribution as reviewer of this work. And to the National Council of Science and Technology National (CONACYT) for supporting the chairs-CONACYT 1048 project.

Cited literature

Butler, C. D. and Trumble, J. T. 2012. The potato psyllid, Bactericera cockerelli (Sulc) Hemiptera: Triozidae): life history, relationship to plant diseases, and management strategies. Terrestrial arthropod reviews. 5(1):87-111. https://doi.org/10.1163/187498312X634266.

Cadena, H. M. A. 1993. La punta morada de la papa en México: Incidencia y búsqueda de resistencia. Agrociencia. 4(2):247-256.

Cadrin, S. X. 2000. Advances in morphometric identification of fishery stocks. Reviews in fish Biology and Fisheries. 10(1):91-112. https://doi.org/10.1023/A:1008939104413.

Camacho-Tapia, M.; Rojas-Martínez, R. I.; Zavaleta-Mejía, E.; Hernández-Deheza, M. G.; Carrillo-Salazar, J. A.; Rebollar-Alviter, A. and Ochoa-Martínez, D. L. 2011. Aetiology of chili pepper variegation from Yurécuaro, México. J. Planth Pathol. 93(2):331-335. http://dx.doi.org/10.4454/jpp.v93i2.1187.

Cerna-Chávez, E.; Hernández-Bautista, O.; Ochoa-Fuentes, Y. M.; Landeros-Flores, J.; Aguirre-Uribe, L.A. y Hernández-Juárez, A. 2018. Morfometría de inmaduros y tablas de vida de Bactericera cockerelli (Hemiptera: Triozidae) de poblaciones del noreste de México. Rev. Colomb. Entomol. 44(1):53-60. http://dx.doi.org/10.25100/socolen.v44i1.6543.

Chapman, R. I.; Macias-Velasco, J. F.; Arp, A. P. and Bextine, B. R. 2012. Using quantitative real time PCR melt curve analysis of partial CO1 sequence for rapid biotype differentiation of Bactericera cockerelli (Hemiptera: Triozidae). Southwest. entomology. 37(4):475-484. https://doi.org/10.3958/059.037.0405.

Delgado-Ortíz, J. C.; Beltrán-Beache, M.; Cerna-Chávez, E.; Aguirre-Uribe, L. A.; Landero-Flores, J.; Rodríguez-Pagaza, Y. y Ochoa-Fuentes, Y. 2019. Candidatus liberibacter solanacearum patógeno vascular de solanáceas: Diagnóstico y control. Rev. Especial. Cienc. Químico-Biológicas. 22(1):1-12. https://doi.org/10.22201/fesz.23958723e.2019. 0.177.

Doyle, J. J. and Doyle, J. L. 1990. Isolation of plant DNA from fresh tissue. Focus. 12(1):13-15.

Greenway, G. A. and Rondon, S. 2018. Economic impacts of zebra chip in idaho, oregon, and washington. American. J. Potato Res. 95(4):362. Doi:10.1007/s12230-018-9636-2.

Gudmestad, N. C. and Secor, G. A. 2007. Zebra chip: a new disease of potato. Nebraska Potato Eyes. 19(1):1-4.

Hardstone, M. C.; Huang, X.; Harringto, L. C. and Scot, J. G. 2010. Differences in development, glycogen, and lipid content associated with cytochrome P450-mediated permethrin resistance in Culex pipiens quinquefasciatus (Diptera: culicidae). J. Medical Entomol. 47(2):188-198. Doi: 10.1603/me09131.

Henrickson, A.; Kalischuk, M.; Lynn, J.; Meers, S.; Johnson, D. and Kawchuk, L. 2019. First report of zebra chip on potato in Canada. Plant Disease. 103(5):1016-1016. https://doi.org/10.1094/PDIS-09-18-1576-PDN.

Hong, L. and Civerolo, E. L. 2014. Genomics of plant-associated bacteria D. C. Gross, A. lichens-park y C. Kole. Springer. New York. 203-234 p. Doi:10.1007/978-3-642-55378-3-9.

Jackson, B. C.; Goolsby, J.; Wyzykowski, A.; Vitovsky, N. and Bextine, B. 2009. Analysis of genetic relationships between potato psyllid (Bactericera cockerelli) populations in the united states, Mexico and guatemala using ITS2 and inter simple sequence repeat (ISSR) data. Plant Sci. 61(1):1-5.

Jirón-Rojas, R. L.; Nava-Camberos, U.; Jiménez-Díaz, F.; Alvarado-Gómez, O. G.; Ávila-Rodríguez, V. y García-Hernández, J. L. 2016. Densidades de Bactericera cockerelli (Sulc) e incidencia del “permanente del tomate” en diferentes condiciones de producción del tomate. Southwestern Entomol. 41(4):1085-1094.

Liefting, L. W.; Sutherland, P. W.; Ward, L. I.; Paice, K. L.; Weir, B. S. and Clover, G. R. 2009. A new ‘Candidatus liberibacter’species associated with diseases of solanaceous crops. Plant Disease. 93(3):208-214. https://doi.org/10.1094/PDIS-93-3-0208.

Liu, D. and Trumble, J. T. 2007. Comparative fitness of invasive and native populations of the potato psyllid (Bactericera cockerelli). Entomologia Experimentalis et Applicata. 123(1):35-42. Doi:10.1111/j.1570-7458.2007.00521.x.

Liu, D.; Trumble, J. T. and Stouthamer. R. 2005. Genetic differentiation between eastern populations and recent introductions of potato psyllid (Bactericera cockerelli) into western north America. Entomologia experimentalis et applicata. 118(3):177-183. https://doi.org/10.1111/j.1570-7458.2006.00383.x.

Loiseau, M.; Garnier, S.; Boirin, V.; Merieau, M.; Leguay, A.; Renaudin, I.; Renvoisé, J. P. and Gentit P. 2014. First report of ‘Candidatus liberibacter solanacearum’ in Carrot in France. Plant Disease. 98(6):839-839. https://doi.org/10.1094/PDIS-08-13-0900-PDN.

Montiel, A. L.; Hail, D.; Macias-Velasco, J. F.; Powell, C. M. and Bextine, B. R. 2016. The mitochondrial genome of the potato psyllid, Bactericera cockerelli sulc., and differences among potato psyllid populations of the United States. Southwestern Entomologist. 41(2):347-360. Doi:10.3958/059.041.0211.

Munyaneza, J. E.; Sengoda, V. G.; Garzón, T. J. A. and Cárdenas, V. O. G. 2009a. First report of “Candidatus liberibacter solanacearum” in tomato plants in Mexico. Plant Disease. 93(10):1076-1076. Doi:10.1094/PDIS-93-10-1076A.

Munyaneza, J. E.; Crosslin, J. M. and Upton, J. E. 2007. Association of bactericera cockerelli (Homoptera: psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. J. Econ. Entomol. 100(3):656-663. Doi: 10.1603/0022-0493(2007) 100[656:aobchp]2.0.co;2.

Munyaneza, J. E. 2010. Psyllids as vectors of emerging bacterial diseases of annual crops. Southwestern entomologist. 35(3):417-477. https://doi.org/10.3958/059.035.0335.

Pletsch, D. J. 1947. The potato psyllid Paratrioza cockerelli (Sulc) its biology and control. Montana Agricultural Experiment Station. Bulletin. 446.

Ramírez-Davila, J. F.; Porcayo-Camargo, E.; Sánchez-Pale, J. R. and Vázquez-García, L. M. 2012. Spatial behavior comparison of bactericera cockerelli sulc. (Hemiptera: triozidae) in Mexico. Neotropical Entomol. 41(1):9-16. http https://doi.org/10.1007/s13744-012-0019-y s://doi.org/10.1007/s13744-012-0019-y.

Ravindran, A.; Levy, J.; Pierson, E. and Gross, D. C. 2011. Development of primers for improved PCR detection of the potato zebra chip pathogen ‘Candidatus liberibacter solanacearum’. Plant Disease. 95(12):1542-1546. Doi:10.1094/PDIS-05-11-0386.

Rubio, C.; Almeyda, L.; Cadena, H. and Lobato, S. 2011. Relation between Bactericera cockerelli and presence of candidatus liberibacter psyllaurous in commercial fields of potato. Rev. Mex. Cienc. Agríc. 2(1):17-28.

Secor, G. A. and Rivera-Varas, V. V. 2004. Emerging diseases of cultivated potato and their impact on latin America. Rev. Latinoamericana de la Papa. 1(1):1-8.

Shufran, K. A. and Payton, T. L. 2009. Limited genetic variation within and between Russian wheat aphid (Hemiptera: Aphididae) biotypes in the United States. J. Econ. Entomol. 102(1):440-445. Doi:10.1603/029.102.0157.

Swisher, K. D.; Arp, A. P.; Bextine, B. R.; Álvarez, E. A.; Crosslin, J. M. and Munyaneza, J. E. 2013. Haplotyping the potato psyllid, Bactericera cockerelli, in Mexico and central America. Southwestern Entomol. 38(2):201-208. https://doi.org/10.3958/059.038.0205.

Swisher, K. D.; Henne, D. C. and Crosslin, J. M. 2014. Identification of a fourth haplotype of Bactericera cockerelli (Hemiptera: Triozidae) in the United States. Fournal Insect Sci. 14(1):1-7. Doi: 10.1093/jisesa/ieu023.

Swisher, K. D.; Munyaneza, J. E. and Crosslin, J. M. 2012. High resolution melting analysis of the cytochrome oxidase I gene identifies three haplotypes of the potato psyllid in the United States. Environ. Entomol. 41(4):1019-1028. https://doi.org/10.1603/EN12066.

Templeton, A. 2006. Scope and basic premises of population genetics. In: Templeton, A. R. (Ed.). Populations genetics and micro evolutionary theory. John Wiley and Sons, Inc. US. 1-18. p Doi:10.1002/0470047356.ch1.

Thinakaran, J.; Pierson, E. A.; Longnecker, M.; Tamborindeguy, C.; Munyaneza, J. E.; Rush, C. M. and Henne, D. C. 2015. Settling and ovipositional behavior of Bactericera cockerelli (Hemiptera: triozidae) on solanaceous hosts under field and laboratory conditions. J. Econ. Entomol. 108(3):904-916. Doi:10.1093/jee/tov058.

Vargas-Madríz, H.; Bautista-Martínez, N.; Vera-Graziano, J.; García-Gutiérrez, C. and Chavarín-Palacio, C. 2013. Morphometrics of eggs, nymphs, and adults of Bactericera cockerelli (Hemiptera: triozidae), grown on two varieties of tomato under greenhouse conditions. Florida Entomologist. 96(1):71-79. https://doi.org/10.1653/024.096.0110.

Vega, G. M. T.; Rodríguez, J. C.; Díaz, G. O.; Bujanos, M. R.; Mota, S. D.; Martínez, C. J. L.; Lagunes, T. A. and Garzón, T. A. 2008. Susceptibilidad a insecticidas en dos poblaciones mexicanas del salerillo, Bactericera cockerelli (Sulc) (Hemiptera: triozidae). Agrociencia. 42(4):463-471.

Yang, X. B. and Liu, T. X. 2009. Life history and life tables of Bactericera cockerelli (Homoptera: Psyllidae) on eggplant and bell pepper. Environ. Entomol. 38(6):1661-1667. Doi:10.1603/022.038.0619.