Evolution of NAC transcription factors from early land plants to domesticated crops

Abstract NAC [NO APICAL MERISTEM (NAM), ARABIDOPSIS TRANSCRIPTION ACTIVATOR FACTOR 1/2 (ATAF1/2), and CUP-SHAPED COTYLEDON (CUC2)] transcription factors are key regulators of plant growth, development, and stress responses but were also crucial players during land plant adaptation and crop domestication. Using representative members of green algae, bryophytes, lycophytes, gymnosperms, and angiosperms, we expanded the evolutionary history of NAC transcription factors to unveil the relationships among members of this gene family. We found a massive increase in the number of NAC transcription factors from green algae to lycophytes and an even larger increase in flowering plants. Many of the NAC clades arose later during evolution since we found eudicot- and monocot-specific clades. Cis-elements analysis in NAC promoters showed the presence of abiotic and biotic stress as well as hormonal response elements, which indicate the ancestral function of NAC transcription factor genes in response to environmental stimuli and in plant development. At the transcriptional level, the expression of NAC transcription factors was low or absent in male reproduction, particularly mature pollen, across the plant kingdom. We also identified NAC genes with conserved expression patterns in response to heat stress in Marchantia polymorpha and Oryza sativa. Our study provides further evidence that transcriptional mechanisms associated with stress responses and development emerged early during plant land adaptation and are still conserved in flowering plants and domesticated crops.