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Review
. 2015 Jul 14:6:535.
doi: 10.3389/fpls.2015.00535. eCollection 2015.

MorTAL Kombat: the story of defense against TAL effectors through loss-of-susceptibility

Mathilde Hutin  1 , Alvaro L Pérez-Quintero  1 , Camilo Lopez  2 , Boris Szurek  1
Affiliations
Review

MorTAL Kombat: the story of defense against TAL effectors through loss-of-susceptibility

Mathilde Hutin et al. Front Plant Sci. .

Erratum in

Abstract

Many plant-pathogenic xanthomonads rely on Transcription Activator-Like (TAL) effectors to colonize their host. This particular family of type III effectors functions as specific plant transcription factors via a programmable DNA-binding domain. Upon binding to the promoters of plant disease susceptibility genes in a sequence-specific manner, the expression of these host genes is induced. However, plants have evolved specific strategies to counter the action of TAL effectors and confer resistance. One mechanism is to avoid the binding of TAL effectors by mutations of their DNA binding sites, resulting in resistance by loss-of-susceptibility. This article reviews our current knowledge of the susceptibility hubs targeted by Xanthomonas TAL effectors, possible evolutionary scenarios for plants to combat the pathogen with loss-of-function alleles, and how this knowledge can be used overall to develop new pathogen-informed breeding strategies and improve crop resistance.

Keywords: TAL effectors; Xanthomonas; agricultural biotechnology; hubs; loss-of-function alleles; plant disease susceptibility S genes.

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Figures

FIGURE 1
FIGURE 1
Functional convergence in bacterial Transcription Activator-Like (TAL) effectors and plant targets. Several susceptibility targets of Xanthomonas oryzae pv. oryzae belong to Clade III of the SWEET family. Four TAL effectors from diverse Xoo strains belonging to different lineages and from distinct geographical origins target OsSWEET14. TalC and Tal5 from the two Xoo African strains BAI3 (Burkina Faso) and MAI1 (Mali) bind to two distinct effector binding elements (EBEs). In addition, the OsSWEET14 promoter is targeted by two Xoo Philippine strains, PXO86 and PXO61 through the TAL effectors AvrXa7 and PthXo3. The corresponding EBEs partially overlap with the Tal5 EBE. The repeat variable di-residue (RVD) arrays and the number of repeats (not represented in the figure) for these three TAL effectors are significantly different, highlighting evolutionary convergence. Not shown in the figure is the case of the resistance gene Xa7 that recognizes AvrXa7 but not PthXo3 that is slightly divergent from AvrXa7. A similar case of convergence is observed for the induction of CsLOB1 which is targeted by PthB and PthC from X. citri ssp. aurantifolii and the PthA series from X. citri ssp. citri. PthA4, PthAw, and PthA∗ (but not PthB and PthC) induce CsSWEET1 belonging to the Clade I of the SWEET family. However, a role in disease development has not been shown. A third species, X. axonopodis pv. manihotis, targets through TAL20 a member of the SWEET family, MeSWEET10a, that belongs to Clade III and acts as a susceptibility gene.
FIGURE 2
FIGURE 2
A simplified model for combat involving bacterial TAL effectors and plant susceptibility genes. To cause disease, bacteria use TAL effectors that bind to the promoter regions of susceptibility (S) genes. The plant might defend itself against these effectors through mutations in the promoter that prevent binding of the TAL effector(s): so called loss-of-susceptibility alleles. Alternatively, plants can trick bacteria into inducing defenses via an executor gene. Bacteria can in turn counter by mutating TAL effectors to recognize the loss-of-susceptibility alleles using for example aberrant repeats that can accommodate single base deletions in the EBE or by mutating TAL effectors to avoid binding to the promoters of executor genes. Bacteria can also acquire new TAL effectors to redundantly induce S genes, the plant can evolve new loss-of-susceptibility alleles and executor genes, and the process becomes cyclical. Bars for plant and bacterium represent “health bars” typically used in video games to indicate the extent to which a combatant is winning or losing. Bold black arrows represent genes.
FIGURE 3
FIGURE 3
Exploiting TAL effector knowledge to identify S genes and loss-of-function alleles. Based on diversity studies conducted on a particular Xanthomonas species, it is possible to direct the research for virulence targets from the most prevalent TAL effectors. Field surveys allow the collection of strains at a regional or national scale. All or representative ones are selected to characterize the TALomes, i.e., their complete repertory of TAL effectors. The corresponding S genes can be identified employing three complementary strategies. First, the expected major virulence role of a prevalent TAL effector has to be assessed in planta (by loss of function mutational analysis or heterologous expression for example). Second, different bioinformatics algorithms (TALVEZ, TAL Effector Nucleotide Targeter, Talgetter) based on the TAL-DNA binding specificity code are employed to predict TAL effector targets in the host genome (assuming that at least a reference genome is available). Finally, RNA profiling strategies are employed to identify TAL effector-dependent differentially expressed genes. Any such genes with a predicted EBE for the TAL effector are strong candidates. For these, functional characterization using designer TAL effectors is the next step (Boch et al., 2014). Then, bioinformatics and functional analyses can be used to identify S hubs. The identification of natural variants in the EBEs from germplasm databases or Ecotilling or the generation of EBE mutations by genome editing in specific EBEs will lead to loss-of-function alleles as new plant disease resistance sources.
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