A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola

Abstract

Summary The rice pathogens Xanthomonas oryzae pathovar (pv.) oryzae and pv. oryzicola produce numerous transcription activator-like (TAL) effectors that increase bacterial virulence by activating expression of host susceptibility genes. Rice resistance mechanisms against TAL effectors include polymorphisms that prevent effector binding to susceptibility gene promoters, or that allow effector activation of resistance genes. This study identifies, in the heirloom variety Carolina Gold Select, a third mechanism of rice resistance involving TAL effectors. This resistance manifests through strong suppression of disease development in response to diverse TAL effectors from both X. oryzae pathovars. The resistance can be triggered by an effector with only 3.5 central repeats, is independent of the composition of the repeat variable diresidues that determine TAL effector binding specificity, and is independent of the transcriptional activation domain. We determined that the resistance is conferred by a single dominant locus, designated Xo1, that maps to a 1.09 Mbp fragment on chromosome 4. The Xo1 interval also confers complete resistance to the strains in the African clade of X. oryzae pv. oryzicola, representing the first dominant resistance locus against bacterial leaf streak in rice. The strong phenotypic similarity between the TAL effector triggered resistance conferred by Xo1 and that conferred by the tomato resistance gene Bs4 suggests that monocots and dicots share an ancient or convergently evolved mechanism to recognize analogous TAL effector epitopes.

Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance

“…Bs4 , a constitutively expressed R gene encoding an NLR protein in tomato, activates resistance including HR in response to the full-length TALE AvrBs4, as well as mutants derived from various truncations of C terminus and truncations of large portion of central repetitive and C-terminal regions that lack the nuclear localization and transcription activation domains of AvrBs4, suggesting cytoplasmic perception of AvrBs4 by Bs4 in tomato1431. Most recently, a locus, Xo1 , mapped in a 1.09 Mbp region in chromosome 4 of the heirloom rice variety Carolina Gold Selection, was found to activate resistance in response to various X. oryzae TALEs and TALE PthXo1 mutant with truncation of its C-terminal transcription activation domain32. Similar to Xa1 , Xo1 -mediated resistance is independent of the number of repeats (if >3.5 repeats) and the composition of the 12th and 13th amino acid residues of each repeat.…”

Effector Mimics and Integrated Decoys, the Never-Ending Arms Race between Rice and Xanthomonas oryzae

“…In response to these defense systems, pathogens have evolved strategies to avoid recognition and suppress plant defenses (Brown and Tellier, 2011). Three recent reports dealing with the resistance of rice to Xanthomonas oryzae have added a new twist to our understanding of this fascinating co-evolutionary arms race (Ji et al, 2016; Read et al, 2016; Triplett et al, 2016). They show that pathogens also develop sophisticated effector mimics to trick recognition.…”

“…Remarkably, two other groups reported the recognition of several TALE effectors by the Xo1 locus a yet uncharacterized gene, which the authors argue to be likely a NLR protein (Read et al, 2016; Triplett et al, 2016). This rather non-specific recognition of TALEs does not lead to broad-spectrum resistance to Xoo and X. oryzae pv.…”

“…These findings provide an exciting novel insight into the evolutionary arms race between plants and pathogens and reveals new functions of TALEs. In these studies, the function of different combinations of TALEs was evaluated by reintroducing them into Xoo strains depleted for most TALEs (Ji et al, 2016; Triplett et al, 2016). The first discovery was that both Xa1 and the newly identified Xo1 locus trigger resistance by recognizing several unrelated X. oryzae TALEs that differ in their target sequence and their number of central repeats (Ji et al, 2016; Triplett et al, 2016).…”

“…However, it appears that at least 3.5 central repeats regardless of their RVDs are required to trigger both Xa1 and Xo1 resistance (Ji et al, 2016; Triplett et al, 2016). Additionally, in the case of Xo1, TALE recognition and activation of resistance does not require the activation domain and is independent of DNA-binding (Read et al, 2016; Triplett et al, 2016). As a consequence, Xa1 recognizes an entire effector family, and not as other NLRs, only individual effectors in a very specific manner.…”