Abstract
Key message
SmZHDs was highly expressed in anthocyanin-rich parts of eggplant. SmZHD12 can activate the expression of SmCHS, SmANS, SmDFR and SmF3H. Overexpression of SmZHD12 promotes anthocyanin biosynthesis in Arabidopsis.
Abstract
The Zinc finger-homeodomain (ZHD) proteins family genes are known to play a significant role in plant development and physiological processes. However, the evolutionary history and function of the ZHD gene family in eggplant remain largely unexplored. This study categorizes a total of 15 SmZHD genes into SmMIF and SmZHD subfamilies based on conserved domains. The phylogeny, gene structure, conserved motifs, promoter elements, and chromosomal locations of the SmZHD genes were comprehensively analyzed. Tissue expression profiles indicate that the majority of SmZHD genes are expressed in anthocyanin-rich areas. qRT-PCR assays revealed distinct expression patterns of SmZHD genes in response to various treatments, indicating their potential involvement in multiple signaling pathways. Analysis of transcriptomic data from light-treated eggplant peel identified SmZHD12 as the most light-responsive gene among the 15 SmZHD genes. Consequently, this study provides further evidence that SmZHD12 facilitates anthocyanin accumulation in Arabidopsis leaves by upregulating the expression of anthocyanin biosynthesis structural genes, as confirmed by dual-luciferase assays and Arabidopsis genetic transformation. Our study will lay a solid foundation for the in-depth study of the involvement of SmZHD genes in the regulation of anthocyanin biosynthesis.
Similar content being viewed by others
Data availability
The datasets supporting the conclusions of this article are included within the article.
References
Banerjee-Basu S, Baxevanis AD (2001) Molecular evolution of the homeodomain family of transcription factors. Nucleic Acids Res 29:3258–3269. https://doi.org/10.1093/nar/29.15.3258
Barchi L, Pietrella M, Venturini L et al (2019) A chromosome-anchored eggplant genome sequence reveals key events in Solanaceae evolution. Sci Rep 9:1–13. https://doi.org/10.1038/s41598-019-47985-w
Cannon SB, Mitra A, Baumgarten A et al (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. https://doi.org/10.1186/1471-2229-4-10
Chen X, Wang P, Gu M et al (2022) Identification of PAL genes related to anthocyanin synthesis in tea plants and its correlation with anthocyanin content. Hortic Plant J 8:381–394. https://doi.org/10.1016/j.hpj.2021.12.005
Chen C, Wu Y, Li J et al (2023) TBtools-II: A “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant 16:1733–1742. https://doi.org/10.1016/j.molp.2023.09.010
Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160
Cirillo V, D’Amelia V, Esposito M et al (2021) Anthocyanins are key regulators of drought stress tolerance in tobacco. Biology (Basel) 10:1–15. https://doi.org/10.3390/biology10020139
Cruz L, Basílio N, Mateus N et al (2022) Natural and synthetic flavylium-based dyes: the chemistry behind the color. Chem Rev 122:1416–1481
Galvão VC, Horrer D, Küttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Dev 139:4072–4082. https://doi.org/10.1242/dev.080879
He Y, Chen H, Zhou L et al (2019) Comparative transcription analysis of photosensitive and non-photosensitive eggplants to identify genes involved in dark regulated anthocyanin synthesis. BMC Genom 20:678. https://doi.org/10.1186/s12864-019-6023-4
He Y, Li DL, Li SH et al (2021a) SmBICs inhibit anthocyanin biosynthesis in eggplant (Solanum melongena L.). Plant Cell Physiol 62:1001–1011. https://doi.org/10.1093/pcp/pcab070
He Y, Wang Z, Ge H et al (2021b) Weighted gene co-expression network analysis identifies genes related to anthocyanin biosynthesis and functional verification of hub gene SmWRKY44. Plant Sci 309:110935. https://doi.org/10.1016/j.plantsci.2021.110935
Heyn P, Kalinka AT, Tomancak P, Neugebauer KM (2015) Introns and gene expression: cellular constraints, transcriptional regulation, and evolutionary consequences. BioEssays 37:148–154. https://doi.org/10.1002/bies.201400138
Hu W, Depamphilis CW, Ma H (2008) Phylogenetic analysis of the plant-specific zinc finger-homeobox and mini zinc finger gene families. J Integr Plant Biol 50:1031–1045. https://doi.org/10.1111/j.1744-7909.2008.00681.x
Hu J, Gao Y, Zhao T et al (2018) Genome-wide identification and expression pattern analysis of zinc-finger homeodomain transcription factors in tomato under abiotic stress. J Am Soc Hortic Sci 143:14–22. https://doi.org/10.21273/JASHS04245-17
Jiang M, Liu Y, Ren L et al (2016) Molecular cloning and characterization of anthocyanin biosynthesis genes in eggplant(Solanum melongena L.). Acta Physiol Plant. https://doi.org/10.1007/s11738-016-2172-0
Jing X, Li C, Luo C et al (2023) Identification and characterization of ZF-HD genes in response to abscisic acid and abiotic stresses in maize. Phyton Int J Exp Bot 92:707–723. https://doi.org/10.32604/phyton.2023.024338
Khatun K, Nath UK, Robin AHK et al (2017) Genome-wide analysis and expression profiling of zinc finger homeodomain (ZHD) family genes reveal likely roles in organ development and stress responses in tomato. BMC Genom. https://doi.org/10.1186/s12864-017-4082-y
Klug A, Schwabe JWR (1995) Protein motifs 5. FASEB J 9:597–604
Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242
Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17. https://doi.org/10.1016/j.envexpbot.2015.05.012
Lev-Yadun S, Gould KS (2008) Role of anthocyanins in plant defence. In: Winefield C, Davies K, Gould K (eds) Anthocyanins. Springer, New York, NY, pp 22–28
Li J, He YJ, Zhou L et al (2018) Transcriptome profiling of genes related to light-induced anthocyanin biosynthesis in eggplant (Solanum melongena L.) before purple color becomes evident. BMC Genom. https://doi.org/10.1186/s12864-018-4587-z
Li L, He Y, Ge H et al (2021) Functional characterization of SmMYB86, a negative regulator of anthocyanin biosynthesis in eggplant(Solanum melongena L.). Plant Sci 302:110696. https://doi.org/10.1016/j.plantsci.2020.110696
Li L, Li S, Ge H et al (2022) A light-responsive transcription factor SmMYB35 enhances anthocyanin biosynthesis in eggplant (Solanum melongena L.). Planta. https://doi.org/10.1007/s00425-021-03698-x
Lila MA (2004) Anthocyanins and human health: an in vitro investigative approach. J Biomed Biotechnol 2004:306–313
Liu Y, Tikunov Y, Schouten RE et al (2018) Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: a review. Front Chem 6:52. https://doi.org/10.3389/fchem.2018.00052
Liu M, Wang X, Sun W et al (2019) Genome-wide investigation of the ZF-HD gene family in tartary buckwheat (Fagopyrum tataricum). BMC Plant Biol. https://doi.org/10.1186/s12870-019-1834-7
Liu Z, Liu Y, Coulter JA et al (2020) The WD40 gene family in potato (Solanum tuberosum L.): genome-wide analysis and identification of anthocyanin and drought-related WD40s. Agronomy. https://doi.org/10.3390/agronomy10030401
Liu H, Yang Y, Zhang L (2021) Zinc finger-homeodomain transcriptional factors (ZF-HDS) in wheat (Triticum aestivum l.): Identification, evolution, expression analysis and response to abiotic stresses. Plants 10:1–15. https://doi.org/10.3390/plants10030593
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lloyd A, Brockman A, Aguirre L et al (2017) Advances in the MYB-bHLH-WD repeat (MBW) pigment regulatory model: addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol 58:1431–1441. https://doi.org/10.1093/pcp/pcx075
Lotkowska ME, Tohge T, Fernie AR et al (2015) The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol 169:1862–1880. https://doi.org/10.1104/pp.15.00605
Mattioli R, Francioso A, Mosca L, Silva P (2020) Anthocyanins: a comprehensive review of their chemical properties and health effects on cardiovascular and neurodegenerative diseases. Molecules. https://doi.org/10.3390/molecules25173809
Mazza CA, Boccalandro HE, Giordano CV et al (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122:117–125. https://doi.org/10.1104/pp.122.1.117
Ngamsamer C, Sirivarasai J, Sutjarit N (2022) The benefits of anthocyanins against obesity-induced inflammation. Biomolecules. https://doi.org/10.3390/biom12060852
Niu SS, Xu CJ, Zhang WS et al (2010) Coordinated regulation of anthocyanin biosynthesis in Chinese bayberry (Myrica rubra) fruit by a R2R3 MYB transcription factor. Planta 231:887–899. https://doi.org/10.1007/s00425-009-1095-z
Niu H, Xia P, Hu Y et al (2021) Genome-wide identification of ZF-HD gene family in Triticum aestivum: molecular evolution mechanism and function analysis. PLoS ONE. https://doi.org/10.1371/journal.pone.0256579
Noman A, Aqeel M, Khalid N et al (2019) Zinc finger protein transcription factors: integrated line of action for plant antimicrobial activity. Microb Pathog 132:141–149
Porri A, Torti S, Romera-Branchat M, Coupland G (2012) Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Dev. https://doi.org/10.1242/dev.077164
Ren L, Hu Z, Li Y et al (2014) Heterologous expression of BoPAP1 in tomato induces stamen specific anthocyanin accumulation and enhances tolerance to a long-term low temperature stress. J Plant Growth Regul 33:757–768. https://doi.org/10.1007/s00344-014-9423-3
Shalmani A, Muhammad I, Sharif R et al (2019) Zinc finger-homeodomain genes: evolution, functional differentiation, and expression profiling under flowering-related treatments and abiotic stresses in plants. Evol Bioinforma. https://doi.org/10.1177/1176934319867930
Sharma M, Kaushik P (2021) Biochemical composition of eggplant fruits: a review. Appl Sci 11:7078
Shen N, Wang T, Gan Q et al (2022) Plant flavonoids: classification, distribution, biosynthesis, and antioxidant activity. Food Chem. https://doi.org/10.1016/j.foodchem.2022.132531
Sun J, Xie M, Li X et al (2021) Systematic investigations of the ZF-HD gene family in tobacco reveal their multiple roles in abiotic stresses. Agronomy. https://doi.org/10.3390/agronomy11030406
Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749
Tian S, Li L, Wei M, Yang F (2019) Genome-wide analysis of basic helix–loop–helix superfamily members related to anthocyanin biosynthesis in eggplant (Solanum melongena L.). PeerJ. https://doi.org/10.7717/peerj.7768
Viola IL, Camoirano A, Gonzalez DH (2016) Redox-dependent modulation of anthocyanin biosynthesis by the TCP transcription factor TCP15 during exposure to high light intensity conditions in Arabidopsis1[OPEN]. Plant Physiol 170:74–85. https://doi.org/10.1104/pp.15.01016
Wang X, Wang X, Hu Q et al (2015) Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis. Plant J 83:300–311. https://doi.org/10.1111/tpj.12887
Wang W, Wu P, Li Y, Hou XL (2016) Genome-wide analysis and expression patterns of ZF-HD transcription factors under different developmental tissues and abiotic stresses in Chinese cabbage. Mol Genet Genomics 291:1451–1464. https://doi.org/10.1007/s00438-015-1136-1
Wang N, Song G, Zhang F et al (2023) Characterization of the WRKY gene family related to anthocyanin biosynthesis and the regulation mechanism under drought stress and methyl jasmonate treatment in Lycoris radiata. Int J Mol Sci. https://doi.org/10.3390/ijms24032423
Windhövel A, Hein I, Dabrowa R, Stockhaus J (2001) Characterization of a novel class of plant homeodomain proteins that bind to the C4 phosphoenolpyruvate carboxylase gene of Flaveria trinervia. Plant Mol Biol 45:201–214. https://doi.org/10.1023/A:1006450005648
Wolberger C (1996) Homeodomain interactions. Curr Opin Struct Biol 6:62–68. https://doi.org/10.1016/S0959-440X(96)80096-0
Xing L, Peng K, Xue S et al (2022) Genome-wide analysis of zinc finger-homeodomain (ZF-HD) transcription factors in diploid and tetraploid cotton. Funct Integr Genom 22:1269–1281. https://doi.org/10.1007/s10142-022-00913-0
Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185
Zhao W, Liu Y, Li L et al (2021) Genome-wide identification and characterization of bHLH transcription factors related to anthocyanin biosynthesis in red walnut (Juglans regia L.). Front Genet. https://doi.org/10.3389/fgene.2021.632509
Zhou L, He Y, Li J et al (2019) CBFs function in anthocyanin biosynthesis by interacting with MYB113 in eggplant (Solanum melongena L.). Plant Cell Physiol 61:416–426. https://doi.org/10.1093/pcp/pcz209
Zhou C, Zhu C, Xie S et al (2021) Genome-wide analysis of zinc finger motif-associated homeodomain (ZF-HD) family genes and their expression profiles under abiotic stresses and phytohormones stimuli in tea plants (Camellia sinensis). Sci Hortic (amsterdam). https://doi.org/10.1016/j.scienta.2021.109976
Acknowledgements
This research was funded by the Natural Science Foundation of Anhui Province, China (2308085QC100) and the National Natural Science Foundation of China (32302583).
Funding
This study was funded by the Innovation training project for college students in Anhui province (S202210364181), the Natural Science Foundation of Anhui Province, China (2308085QC100) and the National Natural Science Foundation of China (32302583).
Author information
Authors and Affiliations
Contributions
QC, XL, HZ, SL and YH conceptualized and orchestrated the research. SL and YH offered the experimental resources. QC, XL and HZ conducted the bioinformatics validation and the experiments. JW, LD and ZZ performed data curation. QC, XL, HZ, JW and YH drafted the manuscript. All authors contributed to the enhancement of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Xian Sheng Zhang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, Q., Liu, X., Zhang, H. et al. Genome-wide characterization of SmZHD gene family and the role of SmZHD12 in regulating anthocyanin biosynthesis in eggplant (Solanum melongena L.). Plant Cell Rep 43, 114 (2024). https://doi.org/10.1007/s00299-024-03195-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00299-024-03195-x