ABSTRACT
The clade III subfamily of OsSWEETs includes transmembrane proteins necessary for susceptibility to bacterial blight (BB). These genes are targeted by the specific transcription activator-like effector (TALE) of Xanthomonas oryzae pv. oryzae and mediate sucrose efflux for bacterial proliferation. However, the mechanism through which OsSWEETs regulate rice immunity has not been fully elucidated. Here, we demonstrated that the cytosolic carboxyl terminus of OsSWEET11a/Xa13 is required for complementing susceptibility to PXO99 in IRBB13 (xa13/xa13). Interestingly, the C-terminus of ZmXa13, the maize homologue of OsSWEET11a/Xa13, could perfectly substitute for the C-terminus of OsSWEET11a/Xa13. Furthermore, OsSWEET11a/Xa13 interacted with the high-mobility group B1 (OsHMGB1) protein and the small heat shock-like protein OsHsp20L through the same regions in the C-terminus. Consistent with the physical interactions, knockdown or knockout of either OsHMGB1 or OsHsp20L caused an enhanced PXO99-resistant phenotype similar to that of OsSWEET11a/OsXa13. Surprisingly, the plants in which OsHMGB1 or OsHsp20L was repressed developed increased resistance to PXO86, PXO61 and YN24, which carry TALEs targeting OsSWEET14/Xa41 or OsSWEET11a/Xa13. Additionally, OsHsp20L can interact with all six members of clade III OsSWEETs, whereas OsHMGB1 can interact with five other members in addition to OsSWEET12. Overall, we revealed that OsHMGB1 and OsHsp20L mediate conserved BB susceptibility by interacting with clade III OsSWEETs, which are candidates for breeding broad-spectrum disease-resistant rice.
Subject(s)
Oryza , Plant Diseases , Plant Immunity , Plant Proteins , Xanthomonas , Oryza/genetics , Oryza/immunology , Oryza/metabolism , Oryza/microbiology , Plant Proteins/genetics , Plant Proteins/metabolism , Plant Diseases/immunology , Plant Diseases/microbiology , Plant Diseases/genetics , Plant Immunity/genetics , HMGB1 Protein/metabolism , HMGB1 Protein/genetics , Gene Expression Regulation, Plant , Disease Resistance/geneticsABSTRACT
BACKGROUND: Bacterial leaf streak (BLS) and bacterial blight (BB) are two major prevalent and devastating rice bacterial diseases caused by the Gram-negative bacteria of Xanthomonas oryzae pv. oryzicola (Xoc) and Xanthomonas oryzae pv. oryzae (Xoo), respectively. Previously, we identified a defence-related (DR) gene encoding a small heat shock protein, OsHsp18.0-CI, that positively regulates BLS and BB resistance in rice. RESULTS: To reveal the regulatory mechanism of the OsHsp18.0-CI response to Xoc and Xoo, we characterized the class B heat shock factor (Hsf), OsHsfB4d, through transcriptional analysis and a transgenic study. OsHsfB4d is upregulated post inoculation by either the Xoc strain RS105 or Xoo strain PXO99a in Zhonghua 11 (wild type, ZH11) as well as in OsHsp18.0-CI overexpressing rice plants. Transient expression of OsHsfB4d can activate the expression of green fluorescent protein (GFP) and luciferase (Luc) via the OsHsp18.0-CI promoter. Rice plants overexpressing OsHsfB4d exhibited enhanced resistance to RS105 and PXO99a as well as increased expression of OsHsp18.0-CI and pathogenesis-related genes. Furthermore, we found that OsHsfB4d directly binds to a DNA fragment carrying the only perfect heat shock element (HSE) in the promoter of OsHsp18.0-CI. CONCLUSION: Overall, we reveal that OsHsfB4d, a class B Hsf, acts as a positive regulator of OsHsp18.0-CI to mediate BLS and BB resistance in rice.
ABSTRACT
BACKGROUND: The small heat shock proteins represent a large family of proteins that respond to a wide range of abiotic and biotic stresses. OsHsp18.0-CI confers tolerance to salt and cadmium and interacts with viral RNA-dependent RNA polymerase (RdRp). However, the direct function of OsHsp18.0-CI in resistance against biotic stresses remains unclear in rice. RESULTS: Here, we report that the expression of OsHsp18.0-CI was up-regulated upon inoculation with RS105, a strain of Xanthomonas oryzae pv. oryzicola (Xoc) that causes bacterial leaf streak in rice. In comparison with wild-type, OsHsp18.0-CI overexpression (OE) lines exhibited enhanced resistance to RS105, whereas repression lines exhibited compromised resistance to RS105. In addition, the transcriptional profiles of wild type and OE lines were compared with and without inoculation with RS105. After inoculation with RS105, most of the genes with up-regulated expression were commonly stimulated in the wild type and OE lines, with stronger induction in the OE lines than in wild type. CONCLUSION: Our study reveals that OsHsp18.0-CI positively regulates resistance to Xoc by mediating an enhanced version of the basal defense response in rice.
