Sex-specific probing behaviour of the carrot psyllid Bactericera trigonica and its implication in the transmission of ‘Candidatus Liberibacter solanacearum’

Abstract

Candidatus Liberibacter solanacearum (Lso)' is a pathogen of Solanaceae but also causes serious physiological disorders in carrots and celery (Apiaceae). In carrots, this pathogen is transmitted by the psyllids Bactericera trigonica and Trioza apicalis. How vector sex influences Lso transmission has not been yet elucidated. Here we report the probing behaviours of male and female B. trigonica and their impact on Lso titre transmitted, percentage of transmission, and symptoms produced on carrots when Lso is transmitted by males or females of B. trigonica. Vector sex affected the inoculation of Lso; our results suggest that females might inoculate higher Lso titres than males. However, the percentage of transmission was not affected by vector sex at a density of one or eight psyllids per plant. The number of yellow leaves and root weight were not different when Lso was transmitted by males or females at either of the psyllid densities tested, except for groups of females whose Lso transmission resulted in a higher number of yellow leaves than did Lso transmitted by groups of males. Electrical penetration graphs (EPG) showed that the proportion of individuals who reached phloem tissues was similar for males and females. However, EPGs also showed that females probed more times, ingested longer from phloem sieve elements and reached phloem tissues more frequently than did males during an 8-h inoculation access period (IAP). Our study shows that differences in probing behaviours between males and females of B. trigonica could modulate how Lso is inoculated by psyllids. These results highlight the importance of taking sex into consideration in psyllid studies of probing behaviour and bacterial transmission.

Transmission of ‘Candidatus Liberibacter solanacearum’ by Bactericera trigonica Hodkinson to vegetable hosts

“…L. asiaticus' transovarial passage or a low rate of transmission is observed in D. citri (Hung et al, 2004;Pelz-Stelinski et al, 2010). In our study, CaLso was detected in 20.3% of eggs laid on carrot by females contaminated with the pathogen, with females are known to probe more times, to ingest longer from phloem sieve elements and to reach phloem tissues more frequently than males (Antolínez et al, 2017a). Thus, the PCR assays showed that the bacterium was vertically transmitted in B. trigonica.…”

“…Only psyllid species that voluntarily land and feed on potato plants would be capable to drive CaLso epidemics. Although the primary transmission from Apiaceae to Solanaceae mediated by B. trigonica would be unlikely, as also considered by Antolínez et al (2017a), we have to keep in mind that B. trigonica is predominant on carrot and celery crops in Spain and is consistently found in potato fields growing in the vicinity (Teresani et al, 2015). The possibility that psyllids will sporadically probe on potato should not be excluded, particularly when potatoes are the only available crop or when the population of psyllids is large, and a whole field of infected carrot or celery is harvested, forcing the population to move to another plant species grown nearby.…”

“…The EPG waveforms of psyllids are reported for D. citri (Bonani et al, 2010;Cen et al, 2012b), B. cockerelli (Butler et al, 2012;Pearson et al, 2014;Sandanayaka et al, 2014;Mustafa et al, 2015), C. pyri L. (Civolani et al, 2011) and Psylla pyricola Förster (Ullman & McLean, 1988). Comparison by EPGs waveforms of the probing behaviours of males and females of B. trigonica in carrot has been recently reported (Antolínez et al, 2017a) and the characterization of the electrical penetration graphs (Antolínez et al, 2017b).…”

“…CaLso is transmitted by Bactericera cockerelli Sulc in potato and tomato (Secor et al, 2009) and by Trioza apicalis Förster in carrot in northern Europe (Nissinen et al, 2014). Bactericera trigonica Hodkinson is associated with vegetative disorders of carrot and celery in Spain (Alfaro-Fernández et al, 2012;Teresani et al, 2014), and Antolínez et al (2017aAntolínez et al ( , 2017b described the feeding behaviour of B. trigonica on carrot plants and reported that the transmission of CaLso was not affected by the vector gender. Moreover, Munyaneza et al (2016) assessed the ability of the potato psyllid B. cockerelli to transmit CaLso from potato to carrot, and Antolínez et al (2017b) the risk of transmission of CaLso from Apiaceae to potato by B. trigonica.…”

Vector mediated transmission of Candidatus Liberibacter solanacearum and epidemiological consequences

“…This technique has been used to correlate psyllid-feeding activities with the transmission of different species of Candidatus Liberibacter (Bonani et al, 2010;;Sandanayaka et al, 2014;Mustafa et al, 2015;Antolínez et al, 2016;Munyaneza et al, 2016). Recently, Munyaneza et al (2016) used EPG to assess the risk of cross transmission of Lso from potato to carrot by the potato psyllid B.…”