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The TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) family proteins are plant-specific transcription factors that have been well-acknowledged for designing the architectures of plant branch, shoot, and inflorescence. However, evidence for their innovation and emerging role in abiotic stress has been lacking. In this study, we identified a total of 36  TCP  genes in  Populus trichocarpa , 50% more than that in  Arabidopsis  (i.e., 24). Comparative intra-genomes showed that such significant innovation was mainly due to the most recent whole genome duplication (rWGD) in  Populus  lineage around Cretaceous-Paleogene (K-Pg) boundary after the divergence from  Arabidopsis . Transcriptome analysis showed that the expressions of  PtrTCP  genes varied among leaf, stem, and root, and they could also be elaborately regulated by abiotic stresses (e.g., cold and salt). Moreover, co-expression network identified a cold-associated regulatory module including  PtrTCP31 ,  PtrTCP10 , and  PtrTCP36 . Of them,  PtrTCP10  was rWGD-duplicated from  PtrTCP31  and evolved a strong capability of cold induction, which might suggest a neofunctionalization of  PtrTCP  genes and contribute to the adaptation of  Populus  lineage during the Cenozoic global cooling. Evidentially, overexpression of  PtrTCP10  into  Arabidopsis  increased freezing tolerance and salt susceptibility. Integrating co-expression network and  cis- regulatory element analysis confirmed that PtrTCP10 can regulate the well-known cold- and salt-relevant genes (e.g.,  ZAT10 ,  GolS2 , and  SOS1 ), proving that PtrTCP10 is an evolutionary innovation in  P. trichocarpa  response to environmental changes. Altogether, our results provide evidence of the rWGD in  P. trichocarpa  responsible for the innovation of  PtrTCP  genes and their emerging roles in environmental stresses.

frontiers in plant science

Innovation and Emerging Roles of Populus trichocarpa TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR Transcription Factors in Abiotic Stresses by Whole-Genome Duplication