June-Sik Kim, Yuki Sakamoto, Fuminori Takahashi, Michitaro Shibata, Kaoru Urano, Sachihiro Matsunaga, Kazuko Yamaguchi-Shinozaki, and Kazuo Shinozaki

PNAS February 8, 2022 119 (6) e2120219119

Significance

Living organisms continuously rebalance their growth and defense/tolerance machineries upon environmental perturbation and energy limitation, which appear as trade-offs. The unfolded protein response (UPR) is a supposed underlying machinery for those trade-offs, responding to a broad spectrum of stress categories and modulating the fundamental growth in both animal and plant systems. We here report the incorporation of general transcription factor NOBIRO6/TAF12b into the UPR-mediated plant root growth control. This indicates that the gene regulation by UPR itself is a key to elucidate the growth trade-offs. Given previously reported roles of NOBIRO6/TAF12b in the signaling of two phytohormones, cytokinin and ethylene, our report proposes how multichannel signals interactively shape plants to survive and thrive in the wild.

Abstract

Plant root growth is indeterminate but continuously responds to environmental changes. We previously reported on the severe root growth defect of a double mutant in bZIP17 and bZIP28 (bz1728) modulating the unfolded protein response (UPR). To elucidate the mechanism by which bz1728 seedlings develop a short root, we obtained a series of bz1728 suppressor mutants, called nobiro, for rescued root growth. We focused here on nobiro6, which is defective in the general transcription factor component TBP-ASSOCIATED FACTOR 12b (TAF12b). The expression of hundreds of genes, including the bZIP60-UPR regulon, was induced in the bz1728 mutant, but these inductions were markedly attenuated in the bz1728nobiro6 mutant. In view of this, we assigned transcriptional cofactor activity via physical interaction with bZIP60 to NOBIRO6/TAF12b. The single nobiro6/taf12b mutant also showed an altered sensitivity to endoplasmic reticulum stress for both UPR and root growth responses, demonstrating that NOBIRO6/TAF12b contributes to environment-responsive root growth control through UPR.

See: https://www.pnas.org/content/119/6/e2120219119

Fig. 1. Characterization of the root growth phenotypes of the bz1728 double mutant. (A and B) Representative image of 10-d-old vertically grown seedlings (A) and their measured primary root lengths (B). (C–E) Representative magnified view of the RAM from 7-d-old primary roots (C), their measured RAM lengths (D), and the corresponding numbers of RAM cells (E). The RAM area was defined from the stem cell niche (lower yellow arrowhead) to the boundary to the EZ (upper yellow arrowhead) along the primary root (C). (F and G) Representative images of cells in the DZ from 7-d-old primary roots (F) and the measured longitudinal lengths of single DZ cells (G). Representative DZ cells are outlined (F). Data are shown with all data points (red circles) and as bar graphs showing the average ± SD from at least 10 seedlings (B) or from root cells of three seedlings (D, E, and G). All presented results are significantly different between WT and bz1728 (Welch’s t test, P < 0.001).