In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin

Authors: ZHANG, SHUAI - China Agricultural University; FENG, MING - China Agricultural University; CHEN, WEN - China Agricultural University; ZHOU, XIAOFANG - China Agricultural University; LU, JINGYUN - China Agricultural University; WANG, YARU - China Agricultural University; LI, YONGBONG - China Agricultural University; Jiang, Cai-Zhong; GAN, SHU-SHENG - Cornell University; MA, NAN - China Agricultural University; GAO, JUNGPING - China Agricultural University

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/25/2019
Publication Date: 3/4/2019
Citation: Zhang, S., Feng, M., Chen, W., Zhou, X., Lu, J., Wang, Y., Li, Y., Jiang, C., Gan, S., Ma, N., Gao, J. 2019. In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin. Nature Plants. 5:290-299. https://doi.org/10.1038/s41477-019-0376-1.
DOI: https://doi.org/10.1038/s41477-019-0376-1

Interpretive Summary: Plants have evolved complex systems to sense and respond to environmental changes, thereby promoting their survival. Growth arrest, especially involving shoot growth inhibition, is a common adaptive response to diverse stress conditions, such as drought and salinity. Growth can slow significantly, and plants can even enter dormancy until more favorable conditions are restored. Regulation of water transport is essential for plants to adapt to stress conditions, and aquaporins (AQPs) provide the major channels for water transport across the plasma membrane and most of intracellular compartments of plant cells. Indeed, AQPs are involved in a broad range of cellular and developmental processes, and appear to be central to both transcriptional and post-translational responses to abiotic stresses. Under water deficiency conditions, the expression of some AQP genes is up-regulated to facilitate water transport and to maintain normal physiological activities, while others may be down-regulated to reduce whole water permeability to avoid excessive water loss. At a post-translational level, channel gating and protein trafficking ensure that AQPs can rapidly respond to multiple stresses. Over the last decade, there has been increasing evidences that AQPs act as a signaling component, rather than only as water channel proteins, since they are capable of transporting hydrogen peroxide (H2O2), which functions as a signal molecule in both animals and plants. In plants, AQPs have been reported to function as H2O2 channels in A. thaliana, Zea may, Nicotiana benthamiana and Tulipa gesneriana, and the ability to transport H2O2 has been reported to be required for plant immunity to the bacterial pathogen Pseudomonas syringae, as well as abscisic acid (ABA)- and pathogen-associated molecular pattern (PAMP) flg22-triggered stomatal closure. However, the mechanisms by which AQPs regulate plant adaptation to environmental stresses are not well understood. In the current study, we tested the hypothesis that PIPs function in plant drought signaling by modulating the subcellular distribution of interacting proteins. Specifically we screened for proteins that interact with the PIP protein, RhPIP2;1, from rose (Rosa sp.). We found that RhPIP2;1 interacts with a membrane-tethered MYB protein, RhPTM. Water deficiency triggers nuclear translocation of RhPTM C-terminus. Silencing of RhPTM causes continuous growth under drought stress, and a consequent decrease in survival rate. RNA-seq indicates that RhPTM influences expression of genes related to carbohydrate metabolism. Water deficiency induces phosphorylation of RhPIP2;1 at Ser273, which is sufficient to promote nuclear translocation of RhPTM C-terminus. These results indicate that RhPIP2;1-RhPTM module serves as a critical player for orchestrating the tradeoff between growth and stress survival in rose.

Technical Abstract: Plants have evolved sophisticated systems to respond to environmental changes, and growth arrest is a common strategy to enhance stress tolerance. Despite the growth-survival tradeoff is essential for shaping plant productivity, the mechanisms balancing growth and survival remain largely unknown. Aquaporins play a crucial role in growth and stress responses by controlling water transport across membranes. Here, we present that RhPIP2;1, an aquaporin from rose (Rosa sp.), interacts with a membrane-tethered MYB protein, RhPTM. Water deficiency triggers nuclear translocation of RhPTM C-terminus. Silencing of RhPTM causes continuous growth under drought stress, and a consequent decrease in survival rate. RNA-seq indicates that RhPTM influences expression of genes related to carbohydrate metabolism. Water deficiency induces phosphorylation of RhPIP2;1 at Ser273, which is sufficient to promote nuclear translocation of RhPTM C-terminus. These results indicate that RhPIP2;1-RhPTM module serves as a critical player for orchestrating the tradeoff between growth and stress survival in rose.