Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato

J. Du, E.C. Verzaux, A. Chaparro-Garcia, G. Bijsterbosch, L.C.P. Keizer, J. Zhou, T.W.H. Liebrand, C. Xie, F. Govers, S. Robatzek, E.A.G. van der Vossen, E. Jacobsen, R.G.F. Visser, S. Kamoun, V.G.A.A. Vleeshouwers

Research output: Contribution to journalArticleAcademicpeer-review

99 Citations (Scopus)

Abstract

Potato late blight, caused by the destructive Irish famine pathogen Phytophthora infestans, is a major threat to global food security1,2. All late blight resistance genes identified to date belong to the coiled-coil, nucleotide-binding, leucine-rich repeat class of intracellular immune receptors3. However, virulent races of the pathogen quickly evolved to evade recognition by these cytoplasmic immune receptors4. Here we demonstrate that the receptor-like protein ELR (elicitin response) from the wild potato Solanum microdontum mediates extracellular recognition of the elicitin domain, a molecular pattern that is conserved in Phytophthora species. ELR associates with the immune co-receptor BAK1/SERK3 and mediates broad-spectrum recognition of elicitin proteins from several Phytophthora species, including four diverse elicitins from P. infestans. Transfer of ELR into cultivated potato resulted in enhanced resistance to P. infestans. Pyramiding cell surface pattern recognition receptors with intracellular immune receptors could maximize the potential of generating a broader and potentially more durable resistance to this devastating plant pathogen.

Potato (Solanum tuberosum L.) is the most important non-grain food crop and a major source of calories for the world's poor5. Increasing potato production is critical to prevent global malnutrition and hunger in an era of expanding world population. Unfortunately, potato suffers from the devastating late blight disease, which is caused by the notorious oomycete pathogen Phytophthora infestans. To limit losses to late blight, potato breeders rely on fungicide treatment and breeding of disease resistance (R) genes, all of which identified thus far belong to the coiled-coil, nucleotide-binding, leucine-rich repeat (CC-NB-LRR) class of immune receptors. These intracellular proteins recognize pathogen avirulence (Avr) proteins of the RxLR class of effectors to mount defence responses. However, RxLR effectors display high evolutionary rates4, and as a result, P. infestans can rapidly circumvent recognition by intracellular R immune receptors, thereby limiting the development of sustainable and durable genetic resistance. Therefore, novel types of immune receptors that recognize a broader spectrum of pathogen molecules are needed.

To fend off pathogens, plants rely on two classes of immune receptors that either reside inside the plant cell (NB-LRRs) or on the cell surface. The first line of defence is initiated by surface receptors, also called pattern recognition receptors (PRRs). PRRs are characteristically receptor-like proteins (RLPs), such as Ve1/Ve26, Cfs7,8 and LeEIX19, or receptor-like kinases (RLKs), such as FLS2, EFR and XA2110. PRRs typically recognize conserved pathogen-associated molecular patterns (PAMPs)11. So far, only a relatively few cell surface receptors against agronomically important pathogens have been identified.

Elicitins are structurally conserved extracellular proteins in Phytophthora and Pythium pathogen species (Pfam PF00964)12,​13,​14. P. infestans contains six elicitin genes that are conserved among different strains13,15. Elicitins are recognized as oomycete PAMPs but their intrinsic function in oomycetes is to bind lipids. Some elicitins sequester sterols from plants, thereby fulfilling an important biological function in Phytophthora and Pythium species that cannot synthesize sterols12. Targeting such conserved ‘Achilles heel’ proteins of pathogens is expected to lead to a more broad-spectrum resistance.

To identify novel types of potential immune receptors against the potato late blight pathogen, we initiated the cloning of ELR, a gene that determines response to elicitins16. We screened a collection of wild Solanum germplasm by Potato virus X (PVX) agroinfection for responses to INF1, a secreted elicitin of P. infestans (Fig. 1a). Solanum microdontum genotype mcd360-1 consistently responded to INF1 with a cell death response (Fig. 1b). We crossed mcd360-1 with S. microdontum ssp. gigantophyllum gig714-1 that does not respond to INF1. The F1 population segregated for response to INF1 in a 1:1 ratio, which suggests that ELR is a single dominant gene.
Original languageEnglish
Article number15034
Number of pages5
JournalNature Plants
Volume1
DOIs
Publication statusPublished - 2015

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