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Article

A Genome-Wide Characterization of Receptor-like Cytoplasmic Kinase IV Subfamily Members in Populus deltoides Identifies the Potential Role of PdeCRCK6 in Plant Osmotic Stress Responses

by
Huanhuan Pan
1,2,†,
Zhengquan He
1,†,
Linxiu Liu
2,
Renyue Cai
3,
Hu Huang
2,
Xinru Xie
2,
Xun Cao
1,2,
Yanan Li
2,
Wenmin Qiu
2,
Zhuchou Lu
2,
Xiaojiao Han
2,
Guirong Qiao
2,
Renying Zhuo
2,
Jianjun Hu
4,* and
Jing Xu
2,*
1
Key Laboratory of Three Gorges Regional Plant Genetic & Germplasm Enhancement (CTGU), Biotechnology Research Center, China Three Gorges University, Yichang 443002, China
2
State Key Laboratory of Tree Genetic and Breeding, The Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou 311400, China
3
Tiantai Forestry Technology Promotion Station, Tiantai 317200, China
4
State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Plants 2024, 13(23), 3371; https://doi.org/10.3390/plants13233371
Submission received: 10 October 2024 / Revised: 21 November 2024 / Accepted: 28 November 2024 / Published: 30 November 2024
(This article belongs to the Special Issue Adaptation Strategies and Defense Mechanisms of Plants During Environmental Stress)
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Abstract

The IV subfamily of receptor-like cytoplasmic kinase (RLCK-IV), known as calcium-binding receptor-like cytoplasmic kinases (CRCKs), plays a vital role in plant signal transduction, particularly in coordinating growth and responses to abiotic stresses. However, our comprehension of CRCK genes in Populus deltoides, a species characterized as fast-growing and pest-resistant but with drought intolerance, is limited. Here, we identify 6 members of the CRCK subfamily on a genome-wide scale in P. deltoides, denoted as PdeCRCK1–PdeCRCK6. An evolutionary and structural analysis revealed highly conserved kinase catalytic domains across all PdeCRCKs, characterized by calmodulin (CaM)-binding sites and serine (Ser)/threonine (Thr) phosphorylation sites. The cis-acting elements of promoters indicated the presence of responsive elements for plant hormones, abiotic stresses, and transcription factor binding sites, which is supported by the distinct transcriptional expression patterns of PdeCRCKs under abscisic acid (ABA), polyethylene glycol (PEG), and mannitol treatments. A transient overexpression of PdeCRCK3/5/6 in tobacco (Nicotiana benthamiana) leaves indicated their involvement in reactive oxygen species (ROS) scavenging, polyamine gene synthesis, and ABA signaling pathway modulation. Immunoprecipitation–Mass Spectrometry (IP–MS) and a yeast two-hybrid (Y2H) assay showed that PdeCRCK6 interacted with AAA-type ATPase proteins and ubiquitin, suggesting its potential function in being involved in chloroplast homeostasis and the 26S ubiquitin protease system. Taken together, these findings offer a comprehensive analysis of the RLCK-IV subfamily members in P. deltoides, especially laying a foundation for revealing the potential mechanism of PdeCRCK6 in response to osmotic stresses and accelerating the molecular design breeding of drought tolerance in poplar.
Keywords: Populus deltoides; RLCK-IV subfamily; CRCK; osmotic stress; gene family Populus deltoides; RLCK-IV subfamily; CRCK; osmotic stress; gene family

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MDPI and ACS Style

Pan, H.; He, Z.; Liu, L.; Cai, R.; Huang, H.; Xie, X.; Cao, X.; Li, Y.; Qiu, W.; Lu, Z.; et al. A Genome-Wide Characterization of Receptor-like Cytoplasmic Kinase IV Subfamily Members in Populus deltoides Identifies the Potential Role of PdeCRCK6 in Plant Osmotic Stress Responses. Plants 2024, 13, 3371. https://doi.org/10.3390/plants13233371

AMA Style

Pan H, He Z, Liu L, Cai R, Huang H, Xie X, Cao X, Li Y, Qiu W, Lu Z, et al. A Genome-Wide Characterization of Receptor-like Cytoplasmic Kinase IV Subfamily Members in Populus deltoides Identifies the Potential Role of PdeCRCK6 in Plant Osmotic Stress Responses. Plants. 2024; 13(23):3371. https://doi.org/10.3390/plants13233371

Chicago/Turabian Style

Pan, Huanhuan, Zhengquan He, Linxiu Liu, Renyue Cai, Hu Huang, Xinru Xie, Xun Cao, Yanan Li, Wenmin Qiu, Zhuchou Lu, and et al. 2024. "A Genome-Wide Characterization of Receptor-like Cytoplasmic Kinase IV Subfamily Members in Populus deltoides Identifies the Potential Role of PdeCRCK6 in Plant Osmotic Stress Responses" Plants 13, no. 23: 3371. https://doi.org/10.3390/plants13233371

APA Style

Pan, H., He, Z., Liu, L., Cai, R., Huang, H., Xie, X., Cao, X., Li, Y., Qiu, W., Lu, Z., Han, X., Qiao, G., Zhuo, R., Hu, J., & Xu, J. (2024). A Genome-Wide Characterization of Receptor-like Cytoplasmic Kinase IV Subfamily Members in Populus deltoides Identifies the Potential Role of PdeCRCK6 in Plant Osmotic Stress Responses. Plants, 13(23), 3371. https://doi.org/10.3390/plants13233371

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