Identification of Autophagy-Related Genes in the Potato Psyllid, Bactericera cockerelli and Their Expression Profile in Response to ‘Candidatus Liberibacter Solanacearum’ in the Gut

Autophagy, also known as type II programmed cell death, is a cellular mechanism of “self-eating”. Autophagy plays an important role against pathogen infection in numerous organisms. Recently, it has been demonstrated that autophagy can be activated and even manipulated by plant viruses to facilitate their transmission within insect vectors. However, little is known about the role of autophagy in the interactions of insect vectors with plant bacterial pathogens. ‘Candidatus Liberibacter solanacearum’ (Lso) is a phloem-limited Gram-negative bacterium that infects crops worldwide. Two Lso haplotypes, LsoA and LsoB, are transmitted by the potato psyllid, Bactericera cockerelli and cause damaging diseases in solanaceous plants (e.g., zebra chip in potatoes). Both LsoA and LsoB are transmitted by the potato psyllid in a persistent circulative manner: they colonize and replicate within psyllid tissues. Following acquisition, the gut is the first organ Lso encounters and could be a barrier for transmission. In this study, we annotated autophagy-related genes (ATGs) from the potato psyllid transcriptome and evaluated their expression in response to Lso infection at the gut interface. In total, 19 ATGs belonging to 17 different families were identified. The comprehensive expression profile analysis revealed that the majority of the ATGs were regulated in the psyllid gut following the exposure or infection to each Lso haplotype, LsoA and LsoB, suggesting a potential role of autophagy in response to Lso at the psyllid gut interface.

Optimizing efficiencies in biosecurity surveillance and monitoring: testing colour and multi-lure traps on tomato potato psyllid, other plant-lice (Psylloidea) and stinkbugs (Pentatomoidea)

Cost efficiency in biosecurity surveillance is vital, and the ability to survey for multiple pest species using just one trap therefore highly appealing. The Psylloidea, or plantlice, contain significant horticultural pest species that act as vectors for a number of deleterious plant bacteriums. We examine the efficacy of using two different coloured sticky traps, and two lure types on the general Psylloidea and Pentatomoidea fauna, and a target extant pest psyllid; tomato potato psyllid (TPP) Bactericera cockerelli (Šulc). Specifically, we test the effect of lure (no lure, Asian citrus psyllid ACP lure, brown marmorated stink bug BMSB lure, combined lures), sticky trap color (green vs yellow), and sentinel plant (tomato vs citrus) on psyllid and stink bug species in 104 urban backyards across Perth, Australia. We found that tomato sentinel host plants and green traps significantly increased the capture rate of TPP, but that all lures decreased the capture of TPP. Green traps also increased the capture rate of all other Psylloidea. Although BMSB lures reduced TPP capture, these lures increased abundances of other Psylloidea and the pest stinkbug Plautia affinis (Dallas) on traps. Thus, our experiment demonstrates that increased efficiencies can be gained with combination traps and lures for particular groups, provided that they have been tested on focal organisms in the first instance, as reactions to non-target lures are unpredictable and species specific.

Bactericera cockerelli (tomato/potato psyllid).

B. cockerelli is one of the most destructive potato pests in the western hemisphere. It was recognized in the early 1900s that B. cockerelli had the potential to be an invasive and harmful insect, particularly in western United States and Mexico (Šulc, 1909; Crawford, 1914; Compere, 1915; 1916; Essig, 1917). By the 1920s and 1930s, B. cockerelli had become a serious and destructive pest of potatoes in most of the southwestern United States, giving rise to the description of a new disease that became known as 'psyllid yellows' (Richards, 1928; 1931; 1933; Binkley, 1929; Richards and Blood, 1933; List and Daniels, 1934; Pletsch, 1947; Wallis, 1955). In recent years, other solanaceous crops, including tomato, pepper, eggplant, tobacco and tamarillo in a number of geographic areas have suffered extensive economic losses associated with B. cockerelli outbreaks (Trumble, 2008, 2009; Munyaneza et al., 2007a, b; 2008; 2009a, b, c, d; Liefting et al., 2008; 2009; Secor et al., 2009; Espinoza, 2010; Munyaneza, 2010; Crosslin et al., 2010; Rehman et al., 2010; Crosslin et al., 2012a, b; Munyaneza, 2012). Despite being a native of North America, B. cockerelli is also found in Central America and has recently invaded New Zealand, where it has caused extensive damage to indoor and outdoor solanaceous crops (Teulon et al., 2009; Thomas et al., 2011). B. cockerelli has recently been placed on the list of quarantine pest in EPPO region (EPPO, 2012).

Liberibacter, A Preemptive Bacterium: Apoptotic Response Repression in the Host Gut at the Early Infection to Facilitate Its Acquisition and Transmission

“Candidatus Liberibacter solanacearum” (Lso) is a phloem-limited Gram-negative bacterium that infects crops worldwide. In North America, two haplotypes of Lso (LsoA and LsoB) are transmitted by the potato psyllid, Bactericera cockerelli (Šulc), in a circulative and persistent manner. Both haplotypes cause damaging plant diseases (e.g., zebra chip in potatoes). The psyllid gut is the first organ Lso encounters and could be a barrier for its transmission. However, little is known about the psyllid gut immune responses triggered upon Lso infection. In this study, we focused on the apoptotic response in the gut of adult potato psyllids at the early stage of Lso infection. We found that there was no evidence of apoptosis induced in the gut of the adult potato psyllids upon infection with either Lso haplotype based on microscopic observations. However, the expression of the inhibitor of apoptosis IAPP5.2 gene (survivin-like) was significantly upregulated during the period that Lso translocated into the gut cells. Interestingly, silencing of IAPP5.2 gene significantly upregulated the expression of two effector caspases and induced apoptosis in the psyllid gut cells. Moreover, RNA interference (RNAi) of IAPP5.2 significantly decreased the Lso titer in the gut of adult psyllids and reduced their transmission efficiency. Taken together, these observations suggest that Lso might repress the apoptotic response in the psyllid guts by inducing the anti-apoptotic gene IAPP5.2 at an early stage of the infection, which may favor Lso acquisition in the gut cells and facilitate its transmission by potato psyllid.

Susceptibility of Physalis longifolia (Solanales: Solanaceae) to Bactericera cockerelli (Hemiptera: Triozidae) and ‘Candidatus Liberibacter solanacearum’

The potato psyllid, Bactericera cockerelli (Šulc), is a major pest of potato (Solanum tuberosum L.; Solanales: Solanaceae) as a vector of ‘Candidatus Liberibacter solanacearum’, the pathogen that causes zebra chip. Management of zebra chip is challenging in part because the noncrop sources of Liberibacter-infected psyllids arriving in potato remain unknown. Adding to this challenge is the occurrence of distinct genetic haplotypes of both potato psyllid and Liberibacter that differ in host range. Longleaf groundcherry (Physalis longifolia Nutt.) has been substantially overlooked in prior research as a potential noncrop source of Liberibacter-infected B. cockerelli colonizing fields of potato. The objective of this study was to assess the suitability of P. longifolia to the three common haplotypes of B. cockerelli (central, western, and northwestern haplotypes), and to two haplotypes of ‘Ca. L. solanacearum’ (Liberibacter A and B haplotypes). Greenhouse bioassays indicated that B. cockerelli of all three haplotypes produced more offspring on P. longifolia than on potato and preferred P. longifolia over potato during settling and egg-laying activities. Greenhouse and field trials showed that P. longifolia was also highly susceptible to Liberibacter. Additionally, we discovered that infected rhizomes survived winter and produced infected plants in late spring that could then be available for psyllid colonization and pathogen acquisition. Results show that P. longifolia is susceptible to both B. cockerelli and ‘Ca. L. solanacearum’ and must be considered as a potentially important source of infective B. cockerelli colonizing potato fields in the western United States.

Tomato Metabolic Changes in Response to Tomato-Potato Psyllid (Bactericera cockerelli) and Its Vectored Pathogen Candidatus Liberibacter solanacearum

The bacterial pathogen ‘Candidatus Liberibacter solanacearum’ (Lso) is transmitted by the tomato potato psyllid (TPP), Bactericera cockerelli, to solanaceous crops. In the present study, the changes in metabolic profiles of insect-susceptible (cv CastleMart) and resistant (RIL LA3952) tomato plants in response to TPP vectoring Lso or not, were examined after 48 h post infestation. Non-volatile and volatile metabolites were identified and quantified using headspace solid-phase microextraction equipped with a gas chromatograph-mass spectrometry (HS-SPME/GC-MS) and ultra-high pressure liquid chromatography coupled to electrospray quadrupole time-of-flight mass spectrometry (UPLC/ESI-HR-QTOFMS), respectively. Partial least squares-discriminant analysis (PLS-DA) was used to define the major uncorrelated metabolite components assuming the treatments as the correlated predictors. Metabolic changes in various classes of metabolites, including volatiles, hormones, and phenolics, were observed in resistant and susceptible plants in response to the insects carrying the pathogen or not. The results suggest the involvement of differentially regulated and, in some cases, implicates antagonistic metabolites in plant defensive signaling. Upon validation, the identified metabolites could be used as markers to screen and select breeding lines with enhanced resistance to reduce economic losses due to the TPP-Lso vector-pathogen complex in Solanaceous crops.