Evolutionary analysis of the bZIP gene family across green plants and its lineage-specific pangenomic landscape in apple ( Malus )

Abstract

The basic leucine zipper (bZIP) transcription factor family plays crucial roles in plant development and stress responses, yet its evolutionary dynamics and functional diversification across green plants remain poorly understood. Here, we conducted a comprehensive analysis of the bZIP family across 114 green plant taxa, from algae to angiosperms, with emphasis on Rosaceae species and Malus accessions. Phylogenetic analysis showed that most bZIP subfamilies formed stable monophyletic clades across green plants, except for two atypical evolutionary patterns. An intertwined E-M-E-I complex suggested that the core domain of subfamily M originated from the group E lineage, whereas the highly divergent subclades, S1 and I1, highlighted the uneven evolutionary rates within the family. In Rosaceae, lineage-specific whole genome duplication (WGD) events, especially in Malinae subtribe and Potentilla, markedly expanded bZIP repertoires with asymmetric retention among subfamilies. Furthermore, lineage-specific pangenome in Malus identified 1251 core and 18 unique bZIP members across diverse accessions. Pan-transcriptome identified tissue-specific expression and stress-responsive co-expression modules. And functional characterization of MP_bZIP77, a gene derived from wild apple, provides a concrete example of this regulatory mechanism by demonstrating that its overexpression enhances salt tolerance through the activation of antioxidant enzyme activities. This study provides novel insights into the evolutionary origin, expansion pattern, and functional divergence of the bZIP family in green plants and Rosaceae, while laying a theoretical and genetic foundation for future molecular breeding aimed at improving stress resistance in fruit trees.