We provide a definitive answer to the question regarding the role of histone H3 lysine 4 tri-methylation marks in the transcription of two ATX1-regulated genes. Despite the proven correlation between the gene transcriptional activity and the level of H3K4me3 modification on the nucleosomes, whether H3K4me3 contributes to, or simply “registers,” active transcription has remained unclear. Another broader-relevance question is whether histone-modifying proteins are required for recruitment of the general transcription machinery, thus playing roles beyond their catalytic activity. Using a combination of gene deletion and specific point mutation analyses, we untangle overlapping effects and reveal that H3K4me3 is not required for TBP/Pol II recruitment to promoters but is critical as an activating mark for transcription elongation. The existing hitherto ambiguity about the role of H3K4me3 as an activating mark has been largely due to the unknown duality of the ATX1/AtCOMPASS functions: facilitating PIC assembly and producing H3K4me3 as an activating mark for transcription elongation.