Hybrid necrosis and hybrid chlorosis are sometimes observed in interspecific hybrids between the tetraploid wheat cultivar Langdon and diploid wild wheat Aegilops tauschii. Many WRKY transcription factor genes are dramatically upregulated in necrosis and chlorosis wheat hybrids. Here, we isolated cDNA clones for four wheat WRKY transcription factor genes, TaWRKY49, TaWRKY92, TaWRKY112, and TaWRKY142, that were commonly upregulated in the hybrid necrosis and hybrid chlorosis and belonged to the same clade of the WRKY gene family. Expression patterns of the four TaWRKY genes in response to several stress conditions were similar in wheat seeding leaves. The four TaWRKY-GFP fusion proteins were targeted to the nucleus in onion epidermal cells. The TaWRKY gene expression levels were increased by high salt, dehydration, darkness, and blast fungus treatment in common wheat. Expression of either of the TaWRKY genes increased salinity and osmotic stress tolerance accompanied with overexpression of STZ/Zat10, and induced overexpression of the salicylic acid-signal pathway marker gene AtPR1 in transgenic Arabidopsis. TaWRKY142 expression also induced the jasmonic acid-pathway marker gene AtPDF1.2 and enhanced resistance against the fungal pathogen Colletotrichum higginsianum in transgenic Arabidopsis. These results suggest that the four TaWRKY genes act as integrated hubs of multiple stress signaling pathways in wheat and play important roles in autoimmune response-inducing hybrid necrosis and hybrid chlorosis.