Evolutionary Consequences of Functional and Regulatory Divergence of HD-Zip I Transcription Factors as a Source of Diversity in Protein Interaction Networks in Plants

Abstract

The HD superfamily has been studied in detail for several decades. The plant-specific HD-Zip I subfamily attracts the most attention because of its involvement in plant development and stress responses. In this review, we provide a comprehensive insight into the evolutionary events responsible for the functional redundancy and diversification of the HD-Zip I genes in regulating various biological processes. We summarized the evolutionary history of the HD-Zip family, highlighting the important role of WGDs in its expansion and divergence of retained duplicates in the genome. To determine the relationship between the evolutionary origin and functional conservation of HD-Zip I in different species, we performed a phylogenetic analysis, compared their expression profiles in different tissues and under stress and traced the role of orthologs and paralogs in regulating developmental processes. We found that HD-Zip I from different species have similar gene structures with a highly conserved HD and Zip, bind to the same DNA sequences and are involved in similar biological processes. However, they exhibit a functional diversity, which is manifested in altered expression patterns. Some of them are involved in the regulation of species-specific leaf morphology and phenotypes. Here, we discuss the role of changes in functional domains involved in DNA binding and protein interaction of HD-Zip I and in cis-regulated regions of its target genes in promoting adaptive innovations through the formation of de novo regulatory systems. Understanding the role of the HD-Zip I subfamily in organism-environment interactions remains a challenge for evolutionary developmental biology (evo-devo).

Keywords: Functional diversity; HD-Zip I subfamily; Plant growth and development; Transcription factors; Whole genome duplication.

Fig. 1

The evolutionary model of the HD-Zip gene family in plants. Major events including duplications (marked by asterisks) or gene loss (marked by lightning), which took place at different stages of the plant evolution, have been shown. The additional domains are colored in red (Color figure online)

Fig. 2

The phylogenetic relationship of the HD-Zip I proteins in plant species based on data collected in PhyloGenes relase (version 3.0) (http://www.phylogenes.org/). Amino acid sequences of the HD-Zip I subfamily were selected from 18 species representing the major plant taxa: Arabidopsis thaliana, Brassica rapa, Brassica napus, Oryza sativa, Hordeum vulgare, Solanum lycopersicum, Solanum tuberosum, Glycine max, Nicotiana tabacum, Medicago truncatula, Triticum aestivum, Zea mays, Junglas regia, Cucumis sativa, Helianthus annuus, Populus trichocarpa, Gossypium hirsutum and Capsicum annuum. The name of genes have been denoted according to the published data: B. rapa (Khan et al. 2018), O. sativa (Agalou et al. 2008), H. vulgare (Li et al. 2019a, b), S. lycopersicum (Zhang et al. 2014), S. tuberosum (Li et al. 2019a, b), G. max (Chen et al. 2014), N. tabacum (Li et al. 2019a, b), M. truncatula (Li et al. 2022), T. aestivum (Yue et al. 2018), Z. mays (Mao et al. 2016), C. sativa (Liu et al. 2013), P. trichocarpa (Hu et al. 2012), G. hirsutum (Zhang et al. 2016) and C. annuum (Zhang et al. 2021). The phylogenetic tree was constructed using MEGA 11 program with the NJ method and 1000 bootstrap replicates. The analyzed proteins were divided into twelve clades designated α, β1, β2, γ, δ, ε, φ1, φ2, ξ and η, and indicated by a specific color (Henriksson et al. ; Li et al. 2019a, b) (Color figure online)

Fig. 3

The transcriptional activity of the HD-Zip I genes in different biological processes in plants. Positive and negative regulatory actions are indicated by red arrows and blue lines with bars, respectively. Two-letter prefixes for sequence identifiers indicate species of origin: Le-Lycopersicon esculentum, At-Arabidopsis thaliana, Mt-Medicago truncatula (Color figure online)

Fig. 4

The model of regulation of various biological processes depending on HD-Zip I. Two-letter prefixes for sequence identifiers indicate species of origin: Le-Lycopersicon esculentum, At-Arabidopsis thaliana, Mt-Medicago truncatula