Orange jasmine as a trap crop to control Diaphorina citri

[EN] Novel, suitable and sustainable alternative control tactics that have the potential to reduce migration of Diaphorina citri into commercial citrus orchards are essential to improve management of huanglongbing (HLB). In this study, the effect of orange jasmine (Murraya paniculata) as a border trap crop on psyllid settlement and dispersal was assessed in citrus orchards. Furthermore, volatile emission profiles and relative attractiveness of both orange jasmine and sweet orange (Citrus¿×¿aurantium L., syn. Citrus sinensis (L.) Osbeck) nursery flushes to D. citri were investigated. In newly established citrus orchards, the trap crop reduced the capture of psyllids in yellow sticky traps and the number of psyllids that settled on citrus trees compared to fallow mowed grass fields by 40% and 83%, respectively. Psyllids were attracted and killed by thiamethoxam-treated orange jasmine suggesting that the trap crop could act as a `sink¿ for D. citri. Additionally, the presence of the trap crop reduced HLB incidence by 43%. Olfactometer experiments showed that orange jasmine plays an attractive role on psyllid behavior and that this attractiveness may be associated with differences in the volatile profiles emitted by orange jasmine in comparison with sweet orange. Results indicated that insecticide-treated M. paniculata may act as a trap crop to attract and kill D. citri before they settled on the edges of citrus orchards, which significantly contributes to the reduction of HLB primary spread.This work was supported by Fund for Citrus Protection (Fundecitrus) and by Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) (Proc. 2015/07011-3). We thank Moacir Celio Vizone, Felipe Marinho Martini and Joao Pedro Ancoma Lopes for technical support with experiments. Furthermore, we thank Cambuhy Agricola Ltda. and University of Araraquara (Uniara) for providing the areas in which the field experiments were performed. Second author received scholarship from National Council for Scientific and Technological Development (CNPq)/Brazil (Proc. 300153/2011-2).Tomaseto, AF.; Marques, RN.; Fereres, A.; Zanardi, OZ.; Volpe, HXL.; Alquézar-García, B.; Peña, L.... (2019). Orange jasmine as a trap crop to control Diaphorina citri. Scientific Reports. 9:1-11. https://doi.org/10.1038/s41598-019-38597-5S1119Bové, J. M. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol. 88, 7–37 (2006).Alvarez, S., Rohrig, E., Solís, D. & Thomas, M. H. Citrus greening disease (Huanglongbing) in Florida: economic impact, management and the potential for biological control. Agric. Res. 5, 109–118 (2016).Belasque, J. Jr. et al. Lessons from huanglongbing management in São Paulo state, Brazil. J. Plant Pathol. 92, 285–302 (2010).Boina, D. R., Meyer, W. L., Onagbola, E. O. & Stelinski, L. L. Quantifying dispersal of Diaphorina citri (Hemiptera: Psyllidae) by immunomarking and potential impact of unmanaged groves on commercial citrus management. Environ. Entomol. 38, 1250–8 (2009).Lewis-Rosenblum, H., Martini, X., Tiwari, S. & Stelinski, L. L. Seasonal movement patterns and long-range dispersal of Asian citrus psyllid in Florida citrus. J. Econ. Entomol. 108, 3–10 (2015).Hall, D. G. & Hentz, M. G. Seasonal flight activity by the Asian citrus psyllid in east central Florida. Entomol. Exp. Appl. 139, 75–85 (2011).Tomaseto, A. F., Krugner, R. & Lopes, J. R. S. Effect of plant barriers and citrus leaf age on dispersal of Diaphorina citri (Hemiptera: Liviidae). J. Appl. Entomol. 140, 91–102 (2016).Gottwald, T. R. Current epidemiological understanding of citrus huanglongbing. Annu. Rev. Phytopathol. 48, 119–139 (2010).Bassanezi, R. B. et al. Efficacy of area-wide inoculum reduction and vector control on temporal progress of huanglongbing in young sweet orange plantings. Plant Dis. 97, 789–796 (2013).Sétamou, M. & Bartels, D. W. Living on the edges: spatial niche occupation of Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), in citrus groves. PLoS One 10, 1–21 (2015).Gottwald, T., Irey, M., Gast, T. & Parnell, S. Spatio-temporal analysis of an HLB epidemic in Florida and implications for spread. In Proceedings of the 17 th Conference of International Organization of Citrus Virologists, IOCV, University of California, Riverside, CA, 84–97 (2010).Shelton, A. M. & Badenes-Perez, F. R. Concepts and applications of trap cropping in pest management. Annu. Rev. Entomol 51, 285–308 (2006).Hokkanen, H. M. T. Trap cropping in pest management. Annu. Rev. Entomol. 36, 119–138 (1991).Stern, V. M., Mueller, A., Sevacherian, V. & Way, M. Lygus bug control in cotton through alfalfa interplanting. Calif. Agric. 8–10 (1969).Godfrey, L. D. & Leigh, T. F. Alfalfa harvest strategy effect on lygus bug (Hemiptera: Miridae) and insect predator population density: Implications for use as trap crop in cotton. Environ. Entomol. 23, 1106–1118 (1994).Gonsalves, D. & Ferreira, S. Transgenic papaya: a case for managing risks of Papaya ringspot virus in Hawaii. Plant Heal. Prog. 1–6, https://doi.org/10.1094/PHP-2003-1113-03-RV (2003)Aubert, B. Trioza erytheae del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of citrus greening disease: biological aspects and possible control strategies. Fruits 42, 149–162 (1987).Leong, S. C. T., Fatimah, A., Beattie, A., Heng, R. K. J. & King, W. S. Influence of host plant species and flush growth stage on the Asian citrus psyllid, Diaphorina citri Kuwayama. Am. J. Agric. Biol. Sci. 6, 536–543 (2011).Patt, J. M. & Sétamou, M. Responses of the Asian citrus psyllid to volatiles emitted by the flushing shoots of its rutaceous host plants. Environ. Entomol. 39, 618–24 (2010).Damsteegt, V. D. et al. Murraya paniculata and related species as potential hosts and inoculum reservoirs of ‘Candidatus Liberibacter asiaticus’, causal agent of huanglongbing. Plant Dis. 94, 528–533 (2010).Lopes, S. A. et al. Liberibacters associated with orange jasmine in Brazil: Incidence in urban areas and relatedness to citrus liberibacters. Plant Pathol. 59, 1044–1053 (2010).Cifuentes-Arenas, J. C. Huanglongbing e Diaphorina citri: Estudos das relações patógeno-vetor-hospedeiro. Ph.D. Thesis. Faculdade de Ciências Agrárias e Veterinárias/Universidade Estadual Paulista (UNESP), Jaboticabal, SP, Brazil. 1–133 (2017).Morilla, G. et al. Pepper (Capsicum annuum) is a dead-end host for Tomato yellow leaf curl virus. Phytopathology 95, 1089–1097 (2005).Midega, C. A. O., Pittchar, J. O., Pickett, J. A., Hailu, G. W. & Khan, Z. R. A climate-adapted push-pull system effectively controls fall armyworm, Spodoptera frugiperda (J. E. Smith), in maize in East Africa. Crop Prot. 105, 10–15 (2018).Miranda, M. P. et al. Processed kaolin affects the probing and settling behavior of Diaphorina citri (Hemiptera: Liviidae). Pest Manag. Sci. 74, 1964–1972 (2018).Kobori, Y., Nakata, T., Ohto, Y. & Takasu, F. Dispersal of adult Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae), the vector of citrus greening disease, in artificial release experiments. Appl. Entomol. Zool. 46, 27–30 (2011).Sétamou, M. et al. Diurnal patterns of flight activity and effects of light on host finding behavior of the Asian citrus psyllid. J. Insect Behav. 25, 264–276 (2012).Wenninger, E. J., Stelinski, L. L. & Hall, D. G. Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ. Entomol. 38, 225–234 (2009).Miranda, M. P., Dos Santos, F. L., Felippe, M. R., Moreno, A. & Fereres, A. Effect of UV-blocking plastic films on take-off and host plant finding ability of Diaphorina citri (Hemiptera: Liviidae). J. Econ. Entomol. 108, 245–251 (2015).Visser, J. H. Host odor perception in phytophagous insects. Annu. Rev. Entomol. 31, 121–144 (1986).Robbins, P. S., Alessandro, R. T., Stelinski, L. L. & Lapointe, S. L. Volatile profiles of young leaves of Rutaceae spp. varying in susceptibility to the Asian citrus psyllid (Hemiptera: Psyllidae). Florida Entomol. 95, 774–776 (2012).Fancelli, M. et al. Attractiveness of host plant volatile extracts to the Asian citrus psyllid, Diaphorina citri, is reduced by terpenoids from the non-host cashew. J. Chem. Ecol. 44, 397–405 (2018).Alquézar, B. et al. β-caryophyllene emitted from a transgenic Arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus Liberibacters. Sci. Rep. 7, 5639 (2017).Jones, R. A. C. Effects of cereal borders, admixture with cereals and plant density on the spread of bean yellow mosaic potyvirus into narrow‐leafed lupins (Lupinus angustifolius). Ann. Appl. Biol. 122, 501–518 (1993).Beloti, V. H., Alves, G. R., Coletta-Filho, H. D. & Yamamoto, P. T. The Asian citrus psyllid host Murraya koenigii is immune to citrus huanglongbing pathogen ‘Candidatus Liberibacter asiaticus’. Phytopathology 108, 1089–1094 (2018).Walter, A. J., Duan, Y. & Hall, D. G. Titers of ‘Ca. Liberibacter asiaticus’ in Murraya paniculata and Murraya-reared Diaphorina citri are much lower than in Citrus and Citrus-reared psyllids. HortScience 47, 1449–1452 (2012).Walter, A. J., Hall, D. G. & Duan, Y. P. Low incidence of ‘Candidatus Liberibacter asiaticus’ in Murraya paniculata and associated Diaphorina citri. Plant Dis. 96, 827–832 (2012).Ammar, E.-D. D., Ramos, J. E., Hall, D. G., Dawson, W. O. & Shatters, R. G. Acquisition, replication and inoculation of Candidatus Liberibacter asiaticus following various acquisition periods on huanglongbing-infected citrus by nymphs and adults of the Asian citrus psyllid. PLoS One 11, e0159594 (2016).Inoue, H. et al. Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Ann. Appl. Biol. 155, 29–36 (2009).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). J. Econ. Entomol. 103, 1531–1541 (2010).Canale, M. C. et al. Latency and persistence of ‘Candidatus Liberibacter asiaticus’ in its psyllid vector, Diaphorina citri (Hemiptera: Liviidae). Phytopathology 107, 264–272 (2017).Li, W., Hartung, J. S. & Levy, L. Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. J. Microbiol. Methods 66, 104–115 (2006).Nakata, T. Effectiveness of micronized fluorescent powder for marking citrus psyllid. Diaphorina citri. Appl. Entomol. Zool. 43, 33–36 (2008).Tomaseto, A. F. et al. Environmental conditions for Diaphorina citri Kuwayama (Hemiptera: Liviidae) take-off. J. Appl. Entomol. 142, 104–113 (2018).Paris, T. M., Croxton, S. D., Stansly, P. A. & Allan, S. A. Temporal response and attraction of Diaphorina citri to visual stimuli. Entomol. Exp. Appl. 155, 137–147 (2015).Zanardi, O. Z. et al. Putative sex pheromone of the Asian citrus psyllid, Diaphorina citri, breaks down into an attractant. Sci. Rep. 8, 455 (2018).Metsalu, T. & Vilo, J. ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 43, W566–W570 (2015).Fournier, D. A. et al. AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim. Methods Softw. 27, 233–249 (2012).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Nelder, J. A. & Wedderburn, R. W. M. Generalized linear models. J. R. Stat. Soc. 135, 370–384 (1972).Demétrio, C. G. B., Hinde, J. & Moral, R. A. In Ecological Modelling Applied to Entomology (eds Ferreira, C. P. & Godoy, W. A. C.) 219–259 (Springer, 2014).Lenth, R. V. Least-Squares Means: the R package lsmeans. J. Stat. Softw. 69, (2016).R Core Team R: A language and environment for statistical computing. 2015. R Foundation for Statistical Computing, Vienna, Austria (2015). Available at, http://www.r-project.org/ . (Accessed: 20th July 2017)

Citrus flush shoot ontogeny modulates biotic potential of <i>Diaphorina citri</i>

<div><p>The biology and behaviour of the psyllid <i>Diaphorina citri</i> Kuwayama (Hemiptera: Sternorrhyncha: Liviidae), the major insect vector of bacteria associated with huanglongbing, have been extensively studied with respect to host preferences, thermal requirements, and responses to visual and chemical volatile stimuli. However, development of the psyllid in relation to the ontogeny of immature citrus flush growth has not been clearly defined or illustrated. Such information is important for determining the timing and frequency of measures used to minimize populations of the psyllid in orchards and spread of HLB. Our objective was to study how flush ontogeny influences the biotic potential of the psyllid. We divided citrus flush growth into six stages within four developmental phases: emergence (V1), development (V2 and V3), maturation (V4 and V5), and dormancy (V6). <i>Diaphorina citri</i> oviposition and nymph development were assessed on all flush stages in a temperature controlled room, and in a screen-house in which ambient temperatures varied. Our results show that biotic potential of <i>Diaphorina citri</i> is not a matter of the size or the age of the flushes (days after budbreak), but the developmental stage within its ontogeny. Females laid eggs on flush V1 to V5 only, with the time needed to commence oviposition increasing with the increasing in flush age. Stages V1, V2 and V3 were most suitable for oviposition, nymph survival and development, and adult emergence, which showed evidence of protandry. Flush shoots at emerging and developmental phases should be the focus of any chemical or biological control strategy to reduce the biotic potential of <i>D</i>. <i>citri</i>, to protect citrus tree from Liberibacter infection and to minimize HLB dissemination.</p></div

Ploidy manipulation and citrus breeding, genetics and genomics

Polyploidy appears to have played a limited role in citrus germplasm evolution. However, today, ploidy manipulation is an important component of citrus breeding strategies. For varieties, the main objective is to develop triploid seedless varieties. For rootstock, the aim is to cumulate interesting traits in tetraploid hybrids and to improve adaptation to biotic and abiotic stresses. In this chapter we make a review of the recent knowledge acquired on the natural mechanisms of citrus polyploidization, and teraploid meiosis. Chromosome doubling of nucellar cells is frequent in apomictic citrus and results in tetraploid seedling production. Unreduced gametes are also frequently produced, mainly by second division restitution for ovules. First division restitution was described for pollen as well as alternative mechanisms for both ovules and pollen. Tetraploid plants display tetrasomic to disomic segregations in relation with their genome structure (autoteraploid versus allotetraploid) and the divergence of the parental species. The implications of the origin of diploid gametes, on the genetic diversity of polyploid progenies, are discussed. The biotechnological tools (haplo-methods, chromosome doubling by chemichal treatments, somatic hybridization and cytogenetic/molecular tools for polyploid genome studies) to optimize ploidy manipulation are presented. The interest of haploids and polyploid genotypes for basic genetic and genomic studies is discussed. The following research area are reviewed: haploids and doubled haploid for genome sequencing and haplotyping, centromere mapping from unreduced gametes, marker-trait association study in polyploids, phenome and gene expression in polyploids with a special focus on polyploidy and adaptation. Finally, we give an overview of the recent advances of concrete polyploid citrus breeding programs in China, Florida and the Mediterranean Basin