Genome-wide characterization of C2H2 zinc-finger gene family provides insight into the mechanisms and evolution of the dehydration–rehydration responses in Physcomitrium and Arabidopsis

Abstract

Dehydration tolerance is a vital factor for land plant evolution and world agricultural production. Numerous studies enlightened that the plant-specific C2H2-type zinc-finger proteins (C2H2-ZFPs) as master regulators played pivotal roles in the abiotic stress responses of plants. However, a comprehensive understanding of the evolution of C2H2-ZFPs in terrestrial plants and its regulatory mechanism in dehydration and rehydration response remains a mystery. In this study, the genome-wide identification of C2H2-ZFP genes revealed 549 homologs in the representatives of terrestrial plant lineages from liverwort to angiosperms. Based on the characteristics of the conserved C2H2-ZF domains, four major C2H2-ZF types (M-, Z-, Q-, and D-type) were identified in the C2H2-ZFPs, with the dominants of M-type in all selected species and followed by Z-type in non-seed plants and Q-type in seed plants, respectively. Phylogenetic analyses of the identified C2H2-ZFPs supported four major groups in the land plant representatives, among which the members from the desiccation-tolerant Physcomitrium patens and the dehydration-sensitive Arabidopsis thaliana displayed different topological relationships in the phylogenies reconstructed for a single species. C2H2-ZFPs clustered in the same subclades shared similar features in their conserved domains and gene structures. Approximately, 81% of the C2H2-ZFP promoters of all 549 identified C2H2-ZFPs harbored the conserved ABA-responsive elements (ABREs) and/or dehydration-responsive elements (DREs). Comparative transcriptomic analyses showed that 50 PpZFPs and 56 AtZFPs significantly changed their transcripts abundance. Interestingly, most of the dehydration- and rehydration-responsive PpZPFs and AtZFPs had been predicted to contain the ABRE and DRE elements in their promoter regions and with over half of which phylogenetically belonging to group III. The differences in the expression patterns of C2H2-ZFPs in responses to dehydration and rehydration between P. patens and A. thaliana reflected their different strategies to adapt to dehydration. The identified candidate PpZFPs were specifically induced by moderate dehydration and reached the peak transcript abundance in severe dehydration. Our study lays the foundations for further functional investigation of C2H2-ZFPs in dehydration responses from an evolutionary perspective in land plants. The findings will provide us with genetic resources and potential targets for drought tolerance breeding in crops and beyond.

A zinc finger transcriptional repressor ZOS5-09 regulates rice grain size, starch and protein biosynthesis

“…This is possible because often there is a balance between different SSPs (Kawakatsu et al, 2010). Similar to our data, where both starch and protein content are affected, opaque3 mutants have decreased protein content and reduced starch accumulation in rice endosperm (Cao et al, 2022). To further support the direct regulation of SSPs by ZOS5-09, we have shown that ZOS5-09 binds to the ZF_BS in the promoter of GLU6 (Fig.…”

“…In addition, they also play important roles in biotic and abiotic stresses (Jiang and Pan, 2012, Han et al ., 2020). Till now, 189 C 2 H 2 ZF proteins have been reported in Oryza sativa (Agarwal et al ., 2007), 122 in Triticum durum (Faraji et al ., 2018), 321 in Glycine max (Yuan et al ., 2018a), 301 in Brassica rapa (Alam et al ., 2019), 104 in Solanum lycopersicum (Hu et al ., 2019), 218 in Medicago truncatula (Jiao et al ., 2020), 129 in Cucumis sativa (Yin et al ., 2020), 79 in Solanum tuberosum (Liu et al ., 2020), 98 in Vitis vinifera (Arrey-Salas et al ., 2021) and 158 in Arabidopsis thaliana (Li et al ., 2022).…”

Analysis of the C2H2 Gene Family in Maize (Zea mays L.) under Cold Stress: Identification and Expression

“…The cis-acting elements of the ZmC2H2 members showed that they had functions related to hormones, stress, and seed germination. As a transcription factor family, C2H2 members have been reported to have a connection with abiotic stresses, such as cold, heat, and drought [ 59 , 60 ]. Moreover, the cis-acting elements also contain hormone-related cis-acting elements, such as salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA), in the C2H2 members’ promoter in poplar ( Populus trichocarpa ) and ginseng ( Panax ginseng ) [ 49 , 61 ].…”

Genome-Wide Analysis of Q-Type C2H2 ZFP Genes in Response to Biotic and Abiotic Stresses in Sugar Beet

“…C2H2-type ZFPs, also known as TFIIIA-type zinc fingers, are among the most extensively studied and abundant ZFPs in eukaryotes [7]. Recently, the in silico genome-wide identification and functional characterization of plant C2H2-type ZFPs were well analyzed in many species, including 321 members in Glycine max [8], 301 in Brassica rapa [9], 218 in Medicago truncatula [10], 204 in Triticum aestivum [11], 189 in Oryza sativa [12], 176 in Arabidopsis thaliana [13], 150 in Zea mays [14], 145 in Sorghum bicolor [15], 129 in Cucumis sativus [16], 109 in Populus trichocarpa [17], and 104 in Solanum lycopersicum [18]. These findings indicate that C2H2 ZFPs are ubiquitous in the plant kingdom, playing important regulatory roles in various biologic processes, including development and organogenesis, as well as responses to stresses and defense.…”