AUTHOR=Wang Shuo , Shen Yirong , Guo Liangyu , Tan Lingling , Ye Xiaoxue , Yang Yanmei , Zhao Xijuan , Nie Yuqi , Deng Deyin , Liu Shenkui , Wu Wenwu 

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

JOURNAL=Frontiers in Plant Science

VOLUME=13

YEAR=2022

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.850064

DOI=10.3389/fpls.2022.850064

ISSN=1664-462X

ABSTRACT=<p>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 <italic>TCP</italic> genes in <italic>Populus trichocarpa</italic>, 50% more than that in <italic>Arabidopsis</italic> (i.e., 24). Comparative intra-genomes showed that such significant innovation was mainly due to the most recent whole genome duplication (rWGD) in <italic>Populus</italic> lineage around Cretaceous-Paleogene (K-Pg) boundary after the divergence from <italic>Arabidopsis</italic>. Transcriptome analysis showed that the expressions of <italic>PtrTCP</italic> 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 <italic>PtrTCP31</italic>, <italic>PtrTCP10</italic>, and <italic>PtrTCP36</italic>. Of them, <italic>PtrTCP10</italic> was rWGD-duplicated from <italic>PtrTCP31</italic> and evolved a strong capability of cold induction, which might suggest a neofunctionalization of <italic>PtrTCP</italic> genes and contribute to the adaptation of <italic>Populus</italic> lineage during the Cenozoic global cooling. Evidentially, overexpression of <italic>PtrTCP10</italic> into <italic>Arabidopsis</italic> increased freezing tolerance and salt susceptibility. Integrating co-expression network and <italic>cis-</italic>regulatory element analysis confirmed that PtrTCP10 can regulate the well-known cold- and salt-relevant genes (e.g., <italic>ZAT10</italic>, <italic>GolS2</italic>, and <italic>SOS1</italic>), proving that PtrTCP10 is an evolutionary innovation in <italic>P. trichocarpa</italic> response to environmental changes. Altogether, our results provide evidence of the rWGD in <italic>P. trichocarpa</italic> responsible for the innovation of <italic>PtrTCP</italic> genes and their emerging roles in environmental stresses.</p>