Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice

Bacterial blight of rice is caused by the -proteobacterium Xanthomonas oryzae pv. oryzae, which utilizes a group of type III TAL (transcription activator-like) effectors to induce host gene expression and condition host susceptibility. Five SWEET genes are functionally redundant to support bacterial disease, but only two were experimentally proven targets of natural TAL effectors. Here, we report the identification of the sucrose transporter gene OsSWEET13 as the disease-susceptibility gene for PthXo2 and the existence of cryptic recessive resistance to PthXo2-dependent X.oryzae pv.oryzae due to promoter variations of OsSWEET13 in japonica rice. PthXo2-containing strains induce OsSWEET13 in indica rice IR24 due to the presence of an unpredicted and undescribed effector binding site not present in the alleles in japonica rice Nipponbare and Kitaake. The specificity of effector-associated gene induction and disease susceptibility is attributable to a single nucleotide polymorphism (SNP), which is also found in a polymorphic allele of OsSWEET13 known as the recessive resistance gene xa25 from the rice cultivar Minghui 63. The mutation of OsSWEET13 with CRISPR/Cas9 technology further corroborates the requirement of OsSWEET13 expression for the state of PthXo2-dependent disease susceptibility to X.oryzae pv.oryzae. Gene profiling of a collection of 104 strains revealed OsSWEET13 induction by 42 isolates of X.oryzae pv.oryzae. Heterologous expression of OsSWEET13 in Nicotiana benthamiana leaf cells elevates sucrose concentrations in the apoplasm. The results corroborate a model whereby X.oryzae pv.oryzae enhances the release of sucrose from host cells in order to exploit the host resources. Significance Statement Two groups of TAL effectors are known to target host disease susceptibility (S) genes for bacterial blight in the field. One group targets OsSWEET11 and the second targets OsSWEET14. Here, we show that the disease susceptibility gene OsSWEET13 is the cognate gene to a highly prevalent third class of TAL effectors represented by PthXo2. Furthermore, japonica subspecies harbor cryptic resistance to blight due to a SNP, which is also present in the recessive resistance gene xa25.