The Conformation of a Plasma Membrane-Localized Somatic Embryogenesis Receptor Kinase Complex Is Altered by a Potato Aphid-Derived Effector

Abstract

Somatic embryogenesis receptor kinases (SERKs) are transmembrane receptors involved in plant immunity. Tomato (Solanum lycopersicum) carries three SERK members. One of these, SlSERK1, is required for Mi-1.2-mediated resistance to potato aphids (Macrosiphum euphorbiae). Mi-1.2 encodes a coiled-coil nucleotide-binding leucine-rich repeat protein that in addition to potato aphids confers resistance to two additional phloem-feeding insects and to root-knot nematodes (Meloidogyne spp.). How SlSERK1 participates in Mi-1.2-mediated resistance is unknown, and no Mi-1.2 cognate pest effectors have been identified. Here, we study the mechanistic involvement of SlSERK1 in Mi-1.2-mediated resistance. We show that potato aphid saliva and protein extracts induce the Mi-1.2 defense marker gene SlWRKY72b, indicating that both saliva and extracts contain a Mi-1.2 recognized effector. Resistant tomato cultivar Motelle (Mi-1.2/Mi-1.2) plants overexpressing SlSERK1 were found to display enhanced resistance to potato aphids. Confocal microscopy revealed that Mi-1.2 localizes at three distinct subcellular compartments: the plasma membrane, cytoplasm, and nucleus. Coimmunoprecipitation experiments in these tomato plants and in Nicotiana benthamiana transiently expressing Mi-1.2 and SlSERK1 showed that Mi-1.2 and SlSERK1 colocalize only in a microsomal complex. Interestingly, bimolecular fluorescence complementation analysis showed that the interaction of Mi-1.2 and SlSERK1 at the plasma membrane distinctively changes in the presence of potato aphid saliva, suggesting a model in which a constitutive complex at the plasma membrane participates in defense signaling upon effector binding.

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

“…The identification of 6A10 as a large subunit ribosomal RNA of B. tabaci deserves further study. There are many examples of the secretion of effector proteins that modulate plant immunity in saliva from hemipterans including aphids and whitefly Will et al, 2013;Sharma et al, 2014;Su et al, 2015;Peng et al, 2016;Villarroel et al, 2016). For instance, the effector proteins C002, Mp1, and Mp2 from aphid promote fecundity, whereas Mp10 and Mp42 decrease fecundity (Bos et al, 2010;Pitino and Hogenhout, 2013).…”

Plant–arthropod interactions: who is the winner?

“…Mi-1.2 from tomato encodes a CC-NB-LRR and confers resistance to the potato aphid, the whitefly B. tabaci, the psyllid Bactericerca cockerelli, and the root-knot nematode Meloidogyne incognita, illustrating the first example of a resistance gene acting against distantly related pests Rossi et al, 1998;Nombela et al, 2003;Casteel et al, 2006). In the presence of potato aphid saliva Mi-1.2 was shown to interact with SlSERK1, a receptor kinase related to Arabidopsis BAK1, and this complex formation is suggested to confer aphid resistance (Peng et al, 2016). Vat from melon is also a CC-NB-LRR and, interestingly, provides dual resistance against the aphid Aphis gossypii and viruses transmitted by this vector (Dogimont et al, 2014).…”

Small RNAs from Bemisia tabaci Are Transferred to Solanum lycopersicum Phloem during Feeding

“…There is evidence that herbivore saliva contains factors that can manipulate plant defenses (Will et al, 2013; Sharma et al, 2014; Su et al, 2015; Peng et al, 2016; Villarroel et al, 2016). For hemipterans most knowledge stems from work with aphids: several salivary proteins (effectors) have been identified that affect aphid reproductive rate (Bos et al, 2010; Pitino and Hogenhout, 2013).…”