The tomato I gene for Fusarium wilt resistance encodes an atypical leucine‐rich repeat receptor‐like protein whose function is nevertheless dependent on SOBIR1 and SERK3/BAK1

Abstract

We have identified the tomato I gene for resistance to the Fusarium wilt fungus Fusarium oxysporum f. sp. lycopersici (Fol) and show that it encodes a membrane-anchored leucine-rich repeat receptor-like protein (LRR-RLP). Unlike most other LRR-RLP genes involved in plant defence, the I gene is not a member of a gene cluster and contains introns in its coding sequence. The I gene encodes a loopout domain larger than those in most other LRR-RLPs, with a distinct composition rich in serine and threonine residues. The I protein also lacks a basic cytosolic domain. Instead, this domain is rich in aromatic residues that could form a second transmembrane domain. The I protein recognises the Fol Avr1 effector protein, but, unlike many other LRR-RLPs, recognition specificity is determined in the C-terminal half of the protein by polymorphic amino acid residues in the LRRs just preceding the loopout domain and in the loopout domain itself. Despite these differences, we show that I/Avr1-dependent necrosis in Nicotiana benthamiana depends on the LRR receptor-like kinases (RLKs) SERK3/BAK1 and SOBIR1. Sequence comparisons revealed that the I protein and other LRR-RLPs involved in plant defence all carry residues in their last LRR and C-terminal LRR capping domain that are conserved with SERK3/BAK1-interacting residues in the same relative positions in the LRR-RLKs BRI1 and PSKR1. Tyrosine mutations of two of these conserved residues, Q922 and T925, abolished I/Avr1-dependent necrosis in N. benthamiana, consistent with similar mutations in BRI1 and PSKR1 preventing their interaction with SERK3/BAK1.

Evidence for horizontal gene transfer and separation of effector recognition from effector function revealed by analysis of effector genes shared between cape gooseberry‐ and tomato‐infecting formae speciales of Fusarium oxysporum

“…SIX1 is recognized at the plasma membrane by the I‐3 SRLK, which confers resistance to Fol races 2 and 3 (Catanzariti et al., ). SIX3 (Avr2) is recognized intracellularly by the I‐2 CC‐NB‐LRR protein, which confers resistance to Fol race 2 (Houterman et al., ; Ma et al ., 2015).SIX4 (Avr1) is recognized at the plasma membrane by the I LRR‐RP, which confers resistance to Fol race 1 (Catanzariti et al., ).…”

“…Several genes for resistance to Fol (I, I-2, I-3 and I-7) have been identified in tomato (Catanzariti et al, 2017;Gonzalez-Cendales et al, 2016;Ori et al, 1997;Simons et al, 1998). I, I-2 and I-3 encode proteins able to recognize specific SIX proteins.…”

“…SIX3 (Avr2) is recognized intracellularly by the I-2 CC-NB-LRR protein, which confers resistance to Fol race 2 Ma et al, 2015). SIX4 (Avr1) is recognized at the plasma membrane by the I LRR-RP, which confers resistance to Fol race 1 (Catanzariti et al, 2017).…”

“…I and I‐7 encode leucine‐rich repeat receptor proteins (LRR RPs), I‐2 encodes a coiled‐coil nucleotide‐binding leucine‐rich repeat (CC‐NB‐LRR) protein and I‐3 encodes an S‐receptor‐like kinase (SRLK). The SIX3 (Avr2) protein is translocated into the plant cell and recognized intracellularly by I‐2 (Houterman et al., ; Ma et al., ), whereas SIX1 (Avr3) and SIX4 (Avr1) are recognized in the apoplast by the plasma membrane‐anchored I‐3 and I RPs, respectively (Catanzariti et al., , ). The effector recognized by I‐7 has not yet been identified, but is likely to be a SIX protein.…”

“…Several genes for resistance to Fol (I, I-2, I-3 and I-7) have been isolated (Catanzariti et al, 2015(Catanzariti et al, , 2017Gonzalez-Cendales et al, 2016;Ori et al, 1997;Simons et al, 1998). I and I-7 encode leucine-rich repeat receptor proteins (LRR RPs), I-2 encodes a coiledcoil nucleotide-binding leucine-rich repeat (CC-NB-LRR) protein and I-3 encodes an S-receptor-like kinase (SRLK).…”