Genome-wide identification of protein kinase family in Populus tomentosa: Functional evidence for causative protein kinase in secondary cell wall biosynthesis

Weina Qi; Mingyang Quan; Yuanyuan Fang; Weixiong Huang; Tailin Ren; Zheng Wen; Liang Xiao; Peng Li; Dan Wang; Qingzhang Du; Qing Liu; Deqiang Zhang

doi:10.1016/j.ijbiomac.2024.138219

Genome-wide identification of protein kinase family in Populus tomentosa: Functional evidence for causative protein kinase in secondary cell wall biosynthesis

Int J Biol Macromol. 2024 Nov 29:138219. doi: 10.1016/j.ijbiomac.2024.138219. Online ahead of print.

Authors

Weina Qi¹, Mingyang Quan¹, Yuanyuan Fang¹, Weixiong Huang¹, Tailin Ren¹, Zheng Wen², Liang Xiao¹, Peng Li¹, Dan Wang¹, Qingzhang Du¹, Qing Liu³, Deqiang Zhang⁴

Affiliations

¹ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China; National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China; Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China.
² State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China.
³ CSIRO Agriculture and Food, Black Mountain, Canberra, ACT 2601, Australia.
⁴ State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China; National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China; Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China. Electronic address: DeqiangZhang@bjfu.edu.cn.

PMID: 39617241
DOI: 10.1016/j.ijbiomac.2024.138219

Abstract

The protein kinase (PK) superfamily holds paramount importance in the plant kingdom, orchestrating myriad cellular processes integral to plant growth, development, as well as resilience against environmental stresses. Nonetheless, the extant biological data about the PK superfamily in perennial woody species remains sparse. In this study, our comprehensive genomic survey of Populus tomentosa unveiled an expansive repertoire of 1543 PK genes, meticulously classified into nine discrete groups and 125 specialized subfamilies. A collinearity analysis revealed that whole genome duplication events served as the preeminent driving forces for PK superfamily expansion. Utilizing cluster analysis of expression profiling in different tissues, we identified 248 PK genes distributed across two clusters implicated in secondary cell wall (SCW) biosynthesis and lignification. Additionally, an association mapping study conducted within a natural population of P. tomentosa pinpointed 176 significant associations, corresponding to 67 PK genes, which were linked to SCW compositional attributes. These findings underscore the genetic determinants shaping PK-mediated modulation of SCW biosynthesis in Populus species. Of particular note, the causative PK gene PtoCMGC48 emerged as a linchpin, exhibiting a pronounced signal associated with lignin content and was found to interact with and phosphorylate the SCW-related transcription factor PtoVND6-C2. This discovery posits a novel molecular paradigm wherein PKs orchestrate SCW biosynthesis via targeted phosphorylation events in P. tomentosa. Overall, our findings lay the groundwork for a deeper appreciation of PK gene functionalities embedded within the complex network governing SCW formation.

Keywords: Phosphorylation; Populus tomentosa; Protein kinase; Regulatory networks; Secondary cell wall.