The Rice TAL Effector–Dependent Resistance Protein XA10 Triggers Cell Death and Calcium Depletion in the Endoplasmic Reticulum

Abstract

The recognition between disease resistance (R) genes in plants and their cognate avirulence (Avr) genes in pathogens can produce a hypersensitive response of localized programmed cell death. However, our knowledge of the early signaling events of the R gene-mediated hypersensitive response in plants remains limited. Here, we report the cloning and characterization of Xa10, a transcription activator-like (TAL) effector-dependent R gene for resistance to bacterial blight in rice (Oryza sativa). Xa10 contains a binding element for the TAL effector AvrXa10 (EBE AvrXa10 ) in its promoter, and AvrXa10 specifically induces Xa10 expression. Expression of Xa10 induces programmed cell death in rice, Nicotiana benthamiana, and mammalian HeLa cells. The Xa10 gene product XA10 localizes as hexamers in the endoplasmic reticulum (ER) and is associated with ER Ca 2+ depletion in plant and HeLa cells. XA10 variants that abolish programmed cell death and ER Ca 2+ depletion in N. benthamiana and HeLa cells also abolish disease resistance in rice. We propose that XA10 is an inducible, intrinsic terminator protein that triggers programmed cell death by a conserved mechanism involving disruption of the ER and cellular Ca 2+ homeostasis.

XA23 Is an Executor R Protein and Confers Broad-Spectrum Disease Resistance in Rice

“…We have analyzed the EBE prediction scores of all the known executor R genes and found that the score for EBE AvrXa23 is more than twice the scores for EBE AvrXa10 , EBE AvrXa27 , EBE AvrBs3 , and EBE AvrBs4 (Supplemental Table 2), indicating that the RVDs of AvrXa23 poorly match to the EBE AvrXa23 sequence. Consistently with the scores, the binding affinities of the cognate TALEs to EBE AvrXa10 , EBE AvrXa27 , EBE AvrBs3 , and EBE AvrBs4 are much stronger (Rö mer et al, 2007;Strauß et al, 2012;Tian et al, 2014) than that between AvrXa23 and EBE AvrXa23 (Figure 6B and 6C).…”

“…These data indicate that XA23 is a homolog of XA10; plant genomes have convergent executor R genes with different EBEs. It has been shown that there are five putative paralogs of XA10 in cultivated and wild rice species but they have not been assigned a function (Tian et al, 2014). One of the paralogs in Nipponbare (National Center for Biotechnology Information accession number ABA94457), which is annotated as a 163-aa protein, is in fact encoded by a predicted gene that is allelic to Xa23 (ORF113).…”

“…The recessive gene xa5 encodes a mutated g subunit of the basal transcription factor IIA on chromosome 5 (TFIIAg5) (Iyer and McCouch, 2004;Jiang et al, 2006); xa13 and xa25 belong to the SWEET multiple gene family (Chu et al, 2006;Liu et al, 2011). As for the dominant R genes, Xa1 encodes an NB-LRR-type protein (Yoshimura et al, 1998); Xa3/Xa26 and Xa21 encode the LRR receptor kinase-type proteins (Song et al, 1995;Sun et al, 2004;Xiang et al, 2006); Xa10 and Xa27 are two executor R genes, encoding, respectively, 126-and 113-aa proteins, with no conserved domains of any known R gene product (Gu et al, 2005;Tian et al, 2014). The resistant allele Xa27 in the rice line IRBB27 and the susceptible allele xa27 in IR24 contain the identical coding sequences but only the resistant allele expresses Xa27 upon infection by Xoo strains expressing AvrXa27, a natural TALE protein (Gu et al, 2005).…”

“…Unlike Xa27, the tested susceptible cultivars (Nipponbare, IR24, IRBB5, and 93-11) do not have an identical open reading frame (ORF) of Xa10. The protein XA10 is localized in the endoplasmic reticulum (ER) and is associated with ER Ca 2+ depletion and induces PCD in rice, Nicotiana benthamiana, and human HeLa cells (Tian et al, 2014).…”

“…Expression of the executor R genes causes programmed cell death (PCD) or a hypersensitive response (HR) in plants, resulting in restriction of pathogen growth and disease resistance phenotypes. Four executor R genes have been cloned, including Xa27 (Gu et al, 2005) and Xa10 (Tian et al, 2014) from rice and Bs3 (Rö mer et al, 2007) and Bs4c (Strauß et al, 2012) from pepper. Unlike other types of plant R genes, the known executor R genes do not share any considerable sequence homology with each other.…”