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

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

doi:10.3389/fpls.2022.850064

Abstract

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.

Highlights

Plant development and defense to various environmental stresses are determined by the coordinate transcriptional regulation of multiple genes
PtrTCP29 and PtrTCP37 have an order of motif 1 followed by motif 2 in contrast to all of the other PtrTCP proteins sharing an order of motifs 2 and 1, demonstrating that PtrTCP29 and PtrTCP37 underwent an evolution of reverse positions of motifs 1 and 2
Comparative genomes showed 50% more TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) genes in P. trichocarpa than in Arabidopsis, and such significant innovation was produced by recent whole genome duplication (rWGD) in Populus lineage after its divergence from Arabidopsis

Summary

Introduction

Plant development and defense to various environmental stresses are determined by the coordinate transcriptional regulation of multiple genes. This is mostly achieved by the action of transcription factors, which show specific DNA binding to regulate downstream genes in response to endogenous and exogenous stimuli (Riechmann et al, 2000). The TCP family is named after the initially identified members, including TEOSINTE BRANCHED1 (TB1) in maize (Zea mays), CYCLOIDEA (CYC) in snapdragon (Antirrhinum majus), and PCF genes in rice (Oryza sativa) (Luo et al, 1996; Doebley et al, 1997; Kosugi and Ohashi, 1997; Cubas et al, 1999), which share a 59-residue conserved non-canonical basic helix-loophelix (bHLH) DNA-binding region (i.e., TCP domain) (Cubas et al, 1999). In addition to the TCP domain, several class II members have an R-domain, which is predicted to form a hydrophilic α-helix or coiled coil structure involved in protein-protein interactions (Lupas et al, 1991)

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