Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

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 or 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.

Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion

“…Tomato plants experiencing different stresses produced exudates that acted as chemoattractants for the beneficial fungus Trichoderma harzianum (Lombardi et al, 2018). Other studies have shown that aphid feeding or whitefly infestation of pepper and tobacco leaves can cause a transcriptional reprogramming in roots and changes in the root microbiome composition which makes plants more resistant to foliar and soilborne pathogens (Yang et al, 2011;Lee et al, 2012;Lee et al, 2018). Recently, Berendsen et al (2018) demonstrated that Arabidopsis leaf infection by the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) can lead to the enrichment of three bacterial taxa (Xanthomonas spp., Stenotrophomonas spp., and Microbacterium spp.)…”

A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance

“…Whitefly, Bemisia tabaci (Hemiptera), is a polyphagous insect and a supervector, transmitting more than 300 plant virus species, that is a threat for many crops across the globe [1]. Whitefly might mediate the suppression of plant defences by secreting protein effectors to improve host colonization and reproductive fitness [6,7]. The whitefly-transmitted monopartite geminivirus begomoviruses are frequently associated with pandemic crop diseases such as tomato yellow leaf curl virus (TYLCV) and tomato yellow leaf curl China virus [8].…”

Spotlight on the Roles of Whitefly Effectors in Insect–Plant Interactions

“…Supplementary Table 1 depicts articles that have been published on aphid, planthopper and psyllid effectors. To date, six studies describing whitefly effectors have been published (Table 1) (Van Kleeff et al, 2016;Yang et al, 2017;Lee et al, 2018;Su et al, 2019;Wang et al, 2019;Xu et al, 2019). These effectors and their in planta locations and modes of action are illustrated in Figures 1A,B, respectively.…”

“…tabaci or P. syringae pv. syringae (Lee et al, 2018). Of the 893 cDNAs tested, three effectors (2G4 and 2G5 encoding proteins with unknown function, and 6A10, a partial transcript of a large subunit ribosomal RNA) were selected using this bioassay.…”

“…However, all three effectors decrease the symptoms induced by R. solanacearum. These effectors, or effector-induced signaling molecules, might be able to translocate between cells, leading to the priming of SAR-related genes (Lee et al, 2018). However, the underlying mechanism has not been further investigated.…”