Bactericera cockerelli resistance in the wild tomato Solanum habrochaites is polygenic and influenced by the presence of Candidatus Liberibacter solanacearum

Abstract

The tomato-potato psyllid (TPP), Bactericera cockerelli, is a vector for the phloem-limited bacterium Candidatus Liberibacter solanacearum (Lso), the causative agent of economically important diseases including tomato vein-greening and potato zebra chip. Here, we screened 11 wild tomato relatives for TPP resistance as potential resources for tomato (Solanum lycopersicum) cultivar development. Six accessions with strong TPP resistance (survival <10%) were identified within S. habrochaites, S. pennelli, S. huaylasense, S. chmielewskii, S. corneliomulleri, and S. galapagense. Two S. pennelli and S. corneliomulleri accessions also showed resistance to Lso. We evaluated recombinant inbred lines (RILs) carrying resistance from S. habrochaites accession LA1777 in the S. lycopersicum background and identified major quantitative trait loci (QTLs) responsible for adult TPP mortality and fecundity in several RILs carrying insertions in different chromosomes, indicating the polygenic nature of these traits. Analysis of a major resistance QTL in RIL LA3952 on chromosome 8 revealed that the presence of Lso is required to increase adult TPP mortality. By contrast, the reduced TPP oviposition trait in LA3952 is independent of Lso. Therefore, resistance traits are available in wild-tomato species, although their complex inheritance and modes of action require further characterisation to optimise their utilisation for tomato improvement.

Figure 1

Tomato-potato psyllid survival on wild tomato species at 10 days after infestation (dai). (1) S. galapagense (LA0528), (2) S. pennellii (LA0716), (3) S. pimpinellifolium (LA0722), (4) S. chmielewskii (LA1028), (5) S. cheesmaniae (LA1037), (6) S. habrochaites (LA1223), (7) S. corneliomulleri (LA1274), (8) S. corneliomulleri (LA1293), (9) S. neorickii (LA1326), (10) S. habrochaites (LA1777), (11) S. pennellii (LA1926), (12) S. chilense (LA1932), (13) S. huaylasense (LA1982), (14) S. arcanum (LA2150), (15) S. arcanum (LA2157), (16) S. chmielewskii (LA2663), (17) S. chilense (LA2884), and (18) S. chilense (LA2930). Mean ± SD labelled with different letters differ significantly at Student’s t-test α = 0.05; n = 3.

Figure 2

Tomato-potato psyllid survival and fecundity on S. habrochaites accession LA1777. Number of (a) alive adults and (b) nymphs and eggs at 10 days after infestation. Means ± SE labelled with different letters differ significantly at Student’s t-test α = 0.05; n = 6.

Figure 3

Tomato-potato psyllid survival and fecundity in S. habrochaites recombinant inbred lines. (A) Adult survival and total number of (B) nymphs and (C) eggs (as a measure of fecundity) at 10 days after inoculation. Red dashed lines indicate values found in the resistance source S. habrochaites LA777. Means ± SE, n = 3–4.

Figure 4

Tomato-potato psyllid survival and fecundity on salicylic acid-deficient plants at 10 days after infestation (dai). Insect (a) survival and (b) fecundity in wild-type tomato cv. MoneyMaker and salicylic acid-deficient transgenic NahG plants. Lso (+) and Lso (−) indicate the presence or absence of Candidatus Liberibacter solanacearum in adult tomato-potato psyllids. Means ± SE labelled with an asterisk (*) differ significantly at Student’s t-test α = 0.05; n = 6.

Figure 5

Intudent’s t-test α = 0.05; n = 6.duction of salicylic acid signaling in response to TPP-Lso infestation. Expression of pathogenesis-related 4 (P4) 48 hours after infestation in (a) susceptible S. lycopersicum and (b) resistant S. habrochaites recombinant inbred line LA3952. Lso (+) and Lso (−) indicate the presence or absence of Candidatus Liberibacter solanacearum in adult tomato-potato psyllids. Means ± SE labelled with different letters differ significantly at Student’s t-test α = 0.05; n = 4.

Figure 6

Tomato-potato psyllid (TPP) fitness in the presence (+) and absence (−) of Candidatus Liberibacter solanacearum (Lso) on S. habrochaites RIL LA3952. Tomato-potato psyllid (a) survival and (b,c) fecundity 10 days after infestation. Means ± SE labelled with different letters differ significantly at Student’s t-test α = 0.05; n = 8.