Evolutionary Relationship of Disease Resistance Genes in Soybean and Arabidopsis Specific for the Pseudomonas syringae Effectors AvrB and AvrRpm1

Abstract

In Arabidopsis (Arabidopsis thaliana), the Pseudomonas syringae effector proteins AvrB and AvrRpm1 are both detected by the RESISTANCE TO PSEUDOMONAS MACULICOLA1 (RPM1) disease resistance (R) protein. By contrast, soybean (Glycine max) can distinguish between these effectors, with AvrB and AvrRpm1 being detected by the Resistance to Pseudomonas glycinea 1b (Rpg1b) and Rpg1r R proteins, respectively. We have been using these genes to investigate the evolution of R gene specificity and have previously identified RPM1 and Rpg1b. Here, we report the cloning of Rpg1r, which, like RPM1 and Rpg1b, encodes a coiledcoil (CC)-nucleotide-binding (NB)-leucine-rich repeat (LRR) protein. As previously found for Rpg1b, we determined that Rpg1r is not orthologous with RPM1, indicating that the ability to detect both AvrB and AvrRpm1 evolved independently in soybean and Arabidopsis. The tightly linked soybean Rpg1b and Rpg1r genes share a close evolutionary relationship, with Rpg1b containing a recombination event that combined a NB domain closely related to Rpg1r with CC and LRR domains from a more distantly related CC-NB-LRR gene. Using structural modeling, we mapped polymorphisms between Rpg1b and Rpg1r onto the predicted tertiary structure of Rpg1b, which revealed highly polymorphic surfaces within both the CC and LRR domains. Assessment of chimeras between Rpg1b and Rpg1r using a transient expression system revealed that AvrB versus AvrRpm1 specificity is determined by the C-terminal portion of the LRR domain. The P. syringae effector AvrRpt2, which targets RPM1 INTERACTOR4 (RIN4) proteins in both Arabidopsis and soybean, partially blocked recognition of both AvrB and AvrRpm1 in soybean, suggesting that both Rpg1b and Rpg1r may detect these effectors via modification of a RIN4 homolog.

Understanding Plant Immunity as a Surveillance System to Detect Invasion

“…The recognition of AvrB by Rpg1b is indirect and requires the presence of one of the four soybean RIN4 homologs (75,131). Detection of AvrRpm1 by Rpg1r also appears to be RIN4 dependent, as expression of AvrRpt2, which can cleave all four soybean RIN4 homologs, mitigates Rpg1r-mediated AvrRpm1 recognition (4,75). Thus, independent from Arabidopsis, soybean evolved a similar mechanism to detect RIN4 perturbation.…”

“…Interestingly, the ability to detect AvrB and AvrRpm1 is not restricted to A. thaliana. In soybean, recognition of both effectors is mediated by the NLRs Resistance to Pseudomonas glycinea 1b and 1r (Rpg1b and Rpg1r), which are nonorthologous to RPM1 (2)(3)(4). The recognition of AvrB by Rpg1b is indirect and requires the presence of one of the four soybean RIN4 homologs (75,131).…”

Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns

“…For example, several CNL genes have been identified in both soybean (Glycine max; Rpg1b and Rpg1r) and Arabidopsis (RPM1 and RPS2) against the bacterial pathogen Pseudomonas syringae by guarding the host protein RIN4 (Bent et al, 1994;Mackey et al, 2002;Mackey et al, 2003;Ashfield et al, 2014). While the Rpg1b and Rpg1r genes were deduced to emerge after the divergence of Fabaceae species, the evolutionary time point of the origin of RPM1 and RPS2 genes in Arabidopsis is largely unknown (Ashfield et al, 2014;Shao et al, 2014). Because all these R genes have likely adopted a similar strategy to defend against the same pathogen, investigating their evolution may elucidate the mechanism underlying the establishment and maintenance of resistance in various plant species.…”

Candidate Gene Sequence Analyses toward Identifying Rsv3‐Type Resistance to Soybean Mosaic Virus

“…1ziw) was used as the template (Choe et al, 2005). Sequence alignment and editing was accomplished as described by Ashfield et al (2014). Four apparent insertions (R565‐S580, E887‐H901, K954‐I971, and D1167‐Q1176) in the Glyma14g38533 sequence that could not be aligned with the TLR3 template structure sequence were subsequently deleted from the model.…”