Systematic evolution of bZIP transcription factors in Malvales and functional exploration of AsbZIP14 and AsbZIP41 in Aquilaria sinensis

Hao Zhang; Xupo Ding; Hao Wang; Huiqin Chen; Wenhua Dong; Jiahong Zhu; Jian Wang; Shiqing Peng; Haofu Dai; Wenli Mei

doi:10.3389/fpls.2023.1243323

Systematic evolution of bZIP transcription factors in Malvales and functional exploration of AsbZIP14 and AsbZIP41 in Aquilaria sinensis

Front Plant Sci. 2023 Aug 30:14:1243323. doi: 10.3389/fpls.2023.1243323. eCollection 2023.

Authors

Hao Zhang¹, Xupo Ding^{1

2}, Hao Wang^{1

2}, Huiqin Chen^{1

2}, Wenhua Dong^{1

2}, Jiahong Zhu^{1

2}, Jian Wang³, Shiqing Peng^{1

2}, Haofu Dai^{1

2}, Wenli Mei^{1

2}

Affiliations

¹ Key Laboratory of Research and Development of Natural Product from Li Folk Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
² Hainan Institute for Tropical Agricultural Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
³ Key Laboratory of Germplasm Resources Biology of Tropical Special Ornamental Plants of Hainan, College of Forestry, Hainan University, Haikou, China.

Abstract

Introduction: Agarwood, the dark-brown resin produced by Aquilaria trees, has been widely used as incense, spice, perfume or traditional medicine and 2-(2-phenethyl) chromones (PECs) are the key markers responsible for agarwood formation. But the biosynthesis and regulatory mechanism of PECs were still not illuminated. The transcription factor of basic leucine zipper (bZIP) presented the pivotal regulatory roles in various secondary metabolites biosynthesis in plants, which might also contribute to regulate PECs biosynthesis. However, molecular evolution and function of bZIP are rarely reported in Malvales plants, especially in Aquilaria trees.

Methods and results: Here, 1,150 bZIPs were comprehensively identified from twelve Malvales and model species genomes and the evolutionary process were subsequently analyzed. Duplication types and collinearity indicated that bZIP is an ancient or conserved TF family and recent whole genome duplication drove its evolution. Interesting is that fewer bZIPs in A. sinensis than that species also experienced two genome duplication events in Malvales. 62 AsbZIPs were divided into 13 subfamilies and gene structures, conservative domains, motifs, cis-elements, and nearby genes of AsbZIPs were further characterized. Seven AsbZIPs in subfamily D were significantly regulated by ethylene and agarwood inducer. As the typical representation of subfamily D, AsbZIP14 and AsbZIP41 were localized in nuclear and potentially regulated PECs biosynthesis by activating or suppressing type III polyketide synthases (PKSs) genes expression via interaction with the AsPKS promoters.

Discussion: Our results provide a basis for molecular evolution of bZIP gene family in Malvales and facilitate the understanding the potential functions of AsbZIP in regulating 2-(2-phenethyl) chromone biosynthesis and agarwood formation.

Keywords: Malvales; agarwood; bZIP; chromone biosynthesis; evolution; transcriptional regulation.

Grants and funding

This work was supported by the National Natural Science Foundation of China (31870668 and 32171824), the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (1630052020003) and the Earmarked Fund of China Agriculture Research System (CARS-21).