Functional characterisation of Dof gene family and expression analysis under abiotic stresses and melatonin-mediated tolerance in pitaya (Selenicereus undatus)
Osama Alam
A # , Latif Ullah Khan B C # , Adeel Khan A , Saleh H. Salmen D , Mohammad Javed Ansari E , Fizza Mehwish A , Mushtaq Ahmad A , Qamar U. Zaman B C * and Hua-Feng Wang B C *
A
B
C
D
E
Handling Editor: Muhammad Nadeem
Abstract
DNA binding proteins with one finger (Dof) transcription factors are essential for seed development and defence against various biotic and abiotic stresses in plants. Genomic analysis of Dof has not been determined yet in pitaya (Selenicereus undatus). In this study, we have identified 26 Dof gene family members, renamed as HuDof-1 to HuDof-26, and clustered them into seven subfamilies based on conserved motifs, domains, and phylogenetic analysis. The gene pairs of Dof family members were duplicated by segmental duplications that faced purifying selection, as indicated by the Ka/Ks ratio values. Promoter regions of HuDof genes contain many cis-acting elements related to phytohormones including abscisic acid, jasmonic acid, gibberellin, temperature, and light. We exposed pitaya plants to different environmental stresses and examined melatonin’s influence on Dof gene expression levels. Signifcant expression of HuDof-2 and HuDof-6 were observed in different developmental stages of flower buds, flowers, pericarp, and pulp. Pitaya plants were subjected to abiotic stresses, and transcriptome analysis was carried out to identify the role of Dof gene family members. RNA-sequencing data and reverse transcription quantitative PCR-based expression analysis revealed three putative candidate genes (HuDof-1, HuDof-2, and HuDof-8), which might have diverse roles against the abiotic stresses. Our study provides a theoretical foundation for functional analysis through traditional and modern biotechnological tools for pitaya trait improvement.
Keywords: abiotic stress tolerance, climate resilience, Dof gene family, dragon fruit (Selenicereus undatus L.), melatonin-mediated tolerance, pitaya, RT-qPCR-based expression analysis, transcriptome analysis.
References
Cai X, Zhang Y, Zhang C, Zhang T, Hu T, Ye J, Zhang J, Wang T, Li H, Ye Z (2013) Genome-wide analysis of plant-specific Dof transcription factor family in tomato. Journal of Integrative Plant Biology 55(6), 552-566.
| Crossref | Google Scholar | PubMed |
Chen Y, Cao J (2015) Comparative analysis of Dof transcription factor family in maize. Plant Molecular Biology Reporter 33, 1245-1258.
| Crossref | Google Scholar |
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13(8), 1194-1202.
| Crossref | Google Scholar | PubMed |
Chen J-Y, Xie F-F, Cui Y-Z, Chen C-B, Lu W-J, Hu X-D, Hua Q-Z, Zhao J, Wu Z-J, Gao D, Zhang Z-K, Jiang W-K, Sun Q-M, Hu G-B, Qin Y-H (2021) A chromosome-scale genome sequence of pitaya (Hylocereus undatus) provides novel insights into the genome evolution and regulation of betalain biosynthesis. Horticulture Research 8, 164.
| Crossref | Google Scholar |
Chen C, Li F, Xie F, Chen J, Hua Q, Chen J, Wu Z, Zhang Z, Zhang R, Zhao J, Hu G, Qin Y (2022a) Pitaya genome and multiomics database (PGMD): a comprehensive and integrative resource of Selenicereus undatus. Genes 13(5), 745.
| Crossref | Google Scholar | PubMed |
Chen C, Xie F, Shah K, Hua Q, Chen J, Zhang Z, Zhao J, Hu G, Qin Y (2022b) Genome-wide identification of WRKY gene family in pitaya reveals the involvement of HmoWRKY42 in betalain biosynthesis. International Journal of Molecular Sciences 23(18), 10568.
| Crossref | Google Scholar | PubMed |
Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Research 14(6), 1188-1190.
| Crossref | Google Scholar | PubMed |
Fornara F, Panigrahi KCS, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Developmental Cell 17(1), 75-86.
| Crossref | Google Scholar | PubMed |
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40(D1), D1178-D1186.
| Crossref | Google Scholar |
Gualberti G, Papi M, Bellucci L, Ricci I, Bouchez D, Camilleri C, Costantino P, Vittorioso P (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. The Plant Cell 14(6), 1253-1263.
| Crossref | Google Scholar | PubMed |
Gupta S, Malviya N, Kushwaha H, Nasim J, Bisht NC, Singh VK, Yadav D (2015) Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241, 549-562.
| Crossref | Google Scholar | PubMed |
Haque E, Taniguchi H, Hassan MM, Bhowmik P, Karim MR, Śmiech M, Zhao K, Rahman M, Islam T (2018) Application of CRISPR/Cas9 genome editing technology for the improvement of crops cultivated in tropical climates: recent progress, prospects, and challenges. Frontiers in Plant Science 9, 617.
| Crossref | Google Scholar | PubMed |
Khan D, Hui L, Khokhar AA, Hussain MA, Lv W, Zaman QU, Wang H-F (2024) Functional characterization of MATE gene family under abiotic stresses and melatonin-mediated tolerance in dragon fruit (Selenicereus undatus L.). Plant Stress 11, 100300.
| Crossref | Google Scholar |
Khatodia S, Bhatotia K, Passricha N, Khurana SMP, Tuteja N (2016) The CRISPR/Cas genome-editing tool: application in improvement of crops. Frontiers in Plant Science 7, 506.
| Crossref | Google Scholar | PubMed |
Khokhar AA, Hui L, Khan D, Hussain MA, Lv W, Zaman QU, Wang H-F (2023) Comprehensive characterization of SBP genes revealed their role under multifactorial stress combinations in dragon fruit (Selenicereus undatus L.). Plant Stress 10, 100294.
| Crossref | Google Scholar |
Konishi M, Yanagisawa S (2007) Sequential activation of two Dof transcription factor gene promoters during vascular development in Arabidopsis thaliana. Plant Physiology and Biochemistry 45(8), 623-629.
| Crossref | Google Scholar | PubMed |
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6), 1547-1549.
| Crossref | Google Scholar | PubMed |
Kushwaha H, Gupta S, Singh VK, Rastogi S, Yadav D (2011) Genome wide identification of Dof transcription factor gene family in sorghum and its comparative phylogenetic analysis with rice and Arabidopsis. Molecular Biology Reports 38, 5037-5053.
| Crossref | Google Scholar | PubMed |
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research 47(W1), W256-W259.
| Crossref | Google Scholar | PubMed |
Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evolutionary Biology 3(1), 17.
| Crossref | Google Scholar |
Lin X, Gao H, Ding Z, Zhan R, Zhou Z, Ming J (2021) Comparative metabolic profiling in pulp and peel of green and red pitayas (Hylocereus polyrhizus and Hylocereus undatus) reveals potential valorization in the pharmaceutical and food industries. BioMed Research International 2021, 6546170.
| Crossref | Google Scholar |
Liu Y, Liu N, Deng X, Liu D, Li M, Cui D, Hu Y, Yan Y (2020) Genome-wide analysis of wheat DNA-binding with one finger (Dof) transcription factor genes: evolutionary characteristics and diverse abiotic stress responses. BMC Genomics 21(1), 276.
| Crossref | Google Scholar |
Marzábal P, Gas E, Fontanet P, Vicente-Carbajosa J, Torrent M, Ludevid MD (2008) The maize Dof protein PBF activates transcription of γ-zein during maize seed development. Plant Molecular Biology 67, 441-454.
| Crossref | Google Scholar | PubMed |
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11(1), 15-19.
| Crossref | Google Scholar | PubMed |
Moreno-Risueno MÁ, Martínez M, Vicente-Carbajosa J, Carbonero P (2007) The family of DOF transcription factors: from green unicellular algae to vascular plants. Molecular Genetics and Genomics 277, 379-390.
| Crossref | Google Scholar | PubMed |
Negi J, Moriwaki K, Konishi M, Yokoyama R, Nakano T, Kusumi K, Hashimoto-Sugimoto M, Schroeder JI, Nishitani K, Yanagisawa S, Iba K (2013) A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Current Biology 23(6), 479-484.
| Crossref | Google Scholar | PubMed |
Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. Plant Science 209, 32-45.
| Crossref | Google Scholar | PubMed |
Paśko P, Galanty A, Zagrodzki P, Ku YG, Luksirikul P, Weisz M, Gorinstein S (2021) Bioactivity and cytotoxicity of different species of pitaya fruits – a comparative study with advanced chemometric analysis. Food Bioscience 40, 100888.
| Crossref | Google Scholar |
Quiroz-González B, García-Mateos R, Corrales-García JJE, Colinas-León MT (2018) Pitaya (Stenocereus spp.): an under-utilized fruit. Journal of the Professional Association for Cactus Development 20, 82-100.
| Crossref | Google Scholar |
Ranganathan S, Simpson KJ, Shaw DC, Nicholas KR (1999) The whey acidic protein family: a new signature motif and three-dimensional structure by comparative modeling. Journal of Molecular Graphics and Modelling 17(2), 106-113.
| Crossref | Google Scholar | PubMed |
Raza A, Salehi H, Rahman MA, Zahid Z, Madadkar Haghjou M, Najafi-Kakavand S, Charagh S, Osman HS, Albaqami M, Zhuang Y, Siddique KHM, Zhuang W (2022) Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Frontiers in Plant Science 13, 961872.
| Crossref | Google Scholar |
Ruiz-Domínguez C, Vovides AP, Sosa V (2019) Systematic relevance of pollen morphology in tribe Hylocereeae (Cactaceae). PhytoKeys 128, 121-140.
| Crossref | Google Scholar | PubMed |
Santos LA, de Souza SR, Fernandes MS (2012) OsDof25 expression alters carbon and nitrogen metabolism in Arabidopsis under high N-supply. Plant Biotechnology Reports 6, 327-337.
| Crossref | Google Scholar |
Schmuths H, Meister A, Horres R, Bachmann K (2004) Genome size variation among accessions of Arabidopsis thaliana. Annals of Botany 93(3), 317-321.
| Crossref | Google Scholar | PubMed |
Senavirathne WMA, Jayatilake DV, Herath V, Wickramasinghe HAM (2017) Evaluation of genetic diversity of cis-acting elements of Abscisic acid responsive element binding protein (ABRE-BP) in selected Sri Lankan rice varieties. Tropical Agricultural Research 28, 120-132.
| Crossref | Google Scholar |
Shah Z, Ahmad S, Ullah A, Munir I, Munir U, Khan A, Sultan W (2024) Insilico-based genome-wide identification and structural characterization of heat shock proteins 70 (HSP70) in cowpea (Vigna unguiculata L.). Genetic Resources and Crop Evolution 71, 1053-1065.
| Crossref | Google Scholar |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13(11), 2498-2504.
| Crossref | Google Scholar | PubMed |
Song Z, Pan F, Lou X, Wang D, Yang C, Zhang B, Zhang H (2019) Genome-wide identification and characterization of Hsp70 gene family in Nicotiana tabacum. Molecular Biology Reports 46(2), 1941-1954.
| Crossref | Google Scholar | PubMed |
Su Y, Liang W, Liu Z, Wang Y, Zhao Y, Ijaz B, Hua J (2017) Overexpression of GhDof1 improved salt and cold tolerance and seed oil content in Gossypium hirsutum. Journal of Plant Physiology 218, 222-234.
| Crossref | Google Scholar | PubMed |
The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400), 635-641.
| Crossref | Google Scholar |
Todeschini A-L, Georges A, Veitia RA (2014) Transcription factors: specific DNA binding and specific gene regulation. Trends in Genetics 30(6), 211-219.
| Crossref | Google Scholar | PubMed |
Umemura Y, Ishiduka T, Yamamoto R, Esaka M (2004) The Dof domain, a zinc finger DNA-binding domain conserved only in higher plants, truly functions as a Cys2/Cys2 Zn finger domain. The Plant Journal 37(5), 741-749.
| Crossref | Google Scholar | PubMed |
Venkatesh J, Park SW (2015) Genome-wide analysis and expression profiling of DNA-binding with one zinc finger (Dof) transcription factor family in potato. Plant Physiology and Biochemistry 94, 73-85.
| Crossref | Google Scholar | PubMed |
Vij S, Gupta V, Kumar D, Vydianathan R, Raghuvanshi S, Khurana P, Khurana JP, Tyagi AK (2006) Decoding the rice genome. BioEssays 28(4), 421-432.
| Crossref | Google Scholar | PubMed |
Wang Y, Wang X, Paterson AH (2012) Genome and gene duplications and gene expression divergence: a view from plants. Annals of the New York Academy of Sciences 1256(1), 1-14.
| Crossref | Google Scholar |
Wang H, Zhao S, Gao Y, Yang J (2017) Characterization of Dof transcription factors and their responses to osmotic stress in poplar (Populus trichocarpa). PLoS ONE 12(1), e0170210.
| Crossref | Google Scholar | PubMed |
Yanagisawa S (2002) The Dof family of plant transcription factors. Trends in Plant Science 7(12), 555-560.
| Crossref | Google Scholar | PubMed |
Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. The Plant Journal 17(2), 209-214.
| Crossref | Google Scholar | PubMed |
Yanagisawa S, Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. The Plant Cell 10(1), 75-89.
| Crossref | Google Scholar | PubMed |
Yang X, Tuskan GA, Cheng (Max) Z-M (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiology 142(3), 820-830.
| Crossref | Google Scholar | PubMed |
Yang J, Yang M-F, Zhang W-P, Chen F, Shen S-H (2011) A putative flowering-time-related Dof transcription factor gene, JcDof3, is controlled by the circadian clock in Jatropha curcas. Plant Science 181(6), 667-674.
| Crossref | Google Scholar | PubMed |
Yu J, Hu S, Wang J, Li S, Wong K-SG, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, et al. (2001) A draft sequence of the rice (Oryza sativa ssp. indica) genome. Chinese Science Bulletin 46, 1937-1942.
| Crossref | Google Scholar |
Zaman QU, Chu W, Hao M, Shi Y, Sun M, Sang S-F, Mei D, Cheng H, Liu J, Li C, Hu Q (2019a) CRISPR/Cas9-mediated multiplex genome editing of JAGGED gene in Brassica napus L. Biomolecules 9(11), 725.
| Crossref | Google Scholar | PubMed |
Zaman QU, Li C, Cheng H, Hu Q (2019b) Genome editing opens a new era of genetic improvement in polyploid crops. The Crop Journal 7(2), 141-150.
| Crossref | Google Scholar |
Zaman QU, Hussain MA, Khan LU, Cui J-P, Hui L, Khan D, Lv W, Wang H-F (2023a) Genome-wide identification and expression pattern of the GRAS gene family in pitaya (Selenicereus undatus L.). Biology 12(1), 11.
| Crossref | Google Scholar | PubMed |
Zaman QU, Hussain MA, Khan LU, Hui L, Khan D, Khokhar AA, Cui J, Raza A, Wang H-F (2023b) Genome-wide identification and expression profiling of APX gene family under multifactorial stress combinations and melatonin-mediated tolerance in pitaya. Scientia Horticulturae 321, 112312.
| Crossref | Google Scholar |
Zaman QU, Khan LU, Hussain MA, Ali A, Hui L, Khokhar AA, Khan D, Wang H-F (2023c) Characterizing the HMA gene family in dragon fruit (Selenicereus undatus L.) and revealing their response to multifactorial stress combinations and melatonin-mediated tolerance. South African Journal of Botany 163, 145-156.
| Crossref | Google Scholar |
Zaman QU, Raza A, Lozano-Juste J, Chao L, Jones MGK, Wang H-F, Varshney RK (2023d) Engineering plants using diverse CRISPR-associated proteins and deregulation of genome-edited crops. Trends in Biotechnology
| Crossref | Google Scholar |
Zhou Y, Cheng Y, Wan C, Li J, Yang Y, Chen J (2020) Genome-wide characterization and expression analysis of the Dof gene family related to abiotic stress in watermelon. PeerJ 8, e8358.
| Crossref | Google Scholar | PubMed |
