Abstract

Infestation of plants with the phloem-feeding whitefly Bemisia tabaci modulates root microbiota and both local and systemic immunity against microbial pathogens. Specifically, aboveground whitefly infestation suppresses pathogen propagation and symptom development caused by the soil-borne pathogens Agrobacterium tumefaciens and Ralstonia solanacearum in the root system through systemic signal transduction. Therefore, we hypothesized that secreted protein(s)/non-protein factors from whitefly saliva (referred to as candidate effectors) might function as insect determinants that activate systemic acquired resistance (SAR) in the host plant. Here, we intensively screened a cDNA library constructed from mRNA from whitefly feeding on Nicotiana benthamiana leaves and selected three candidate effectors, 2G4, 2G5, and 6A10, that appear to reduce disease development caused by the aboveground pathogen Pseudomonas syringae pv. tabaci and the soil-borne pathogen R. solanacearum. Transient expression of the three candidate effector cDNAs in leaves primed the expression of SAR marker genes NbPR1a and NbPR2 in local and systemic leaves against P. syringae pv. tabaci, while leaf infiltration with 2G4 and 6A10 cDNA elicited strong defense priming of SAR markers following drench application of R. solanacearum on plant roots. In silico and qRT-PCR analyses revealed the presence of 2G5 and 6A10 transcripts in insect salivary glands. This is the first report of whitefly effectors that prime SAR against aboveground and belowground bacterial pathogens.

Highlights

  • Plants are constantly exposed to diverse insect pests and microbial pathogens (Agrios, 2005)

  • We evaluated whether the three candidate effectors would elicit plant immunity in local or systemic tissues of N. benthamiana

  • On day 5 after pathogen challenge in leaves infiltrated with the three candidate effectors, the number of bacteria was not statistically different among systemic leaves while they differed compared to empty vector control on day 3 (Figure 2G), and the number of bacteria was similar to that of the BTH-pretreated positive control in local leaves (Figures 2F,G)

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Summary

Introduction

Plants are constantly exposed to diverse insect pests and microbial pathogens (Agrios, 2005). To protect from these enemies, immune responses, including chemical and physical defense mechanisms, are activated in local and systemic plant tissues (Koornneef and Pieterse, 2008; Dangl et al, 2013). Aboveground (leaf) whitefly infestation increases plant immunity against soil-borne plant pathogens, indicating that systemic plant signaling is activated and translocated from leaf to root. Whitefly-elicited plant immunity in pepper activates both SAand jasmonic acid (JA)-related gene expression in aboveground and belowground tissue, indicating that SA- and JA-dependent pathways are activated from leaf to root in response to whitefly feeding on leaves (Park and Ryu, 2014). Further investigation involving the fine-tuning of these signaling pathways following whitefly infestation using virus-induced gene knockdown of SAand JA-responsive and biosynthesis genes revealed that SA is a major player in whitefly feeding-dependent signaling (Lazebnik et al, 2014; Song et al, 2015)

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