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Genome-wide identification of the Carya illinoinensis bZIP transcription factor and the potential function of S1-bZIPs in abiotic stresses

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Abstract 

The basic leucine zipper (bZIP) is a transcription factor broadly found in higher plants and is involved in numerous crucial physiological processes: growth and development, stress responses, etc. The pecan (Carya illinoinensis) is a highly ornamental and economical woody plant that is popular in landscape and economic forestry. However, the identification and analysis of the bZIP TF system in pecan have not been reported. To acquire information on the bZIP gene family in pecan, we appraised 77 members of the bZIP gene family from the pecan genome and categorized them into 12 subfamilies (S, B, A, D, F, E, G, I, J, H, K, and C) using bioinformatics methods. Analysis in terms of gene structure and conserved motif composition revealed that each subtribe shares a comparable number of introns-exons and functions. Ka/Ks results suggested that bZIP evolution was influenced by purifying selection. The promoter cis-acting element analysis revealed a huge number of abscisic acid–responsive elements, light-responsive elements, and jasmonic acid–responsive elements in pecan bZIPs. Furthermore, the protein interaction network predicted a possible role for S1-bZIPs in abiotic stress, and the qRT-PCR results further demonstrated that this subpopulation responds to abiotic stress. Meanwhile, the results of subcellular localization and transcriptional activity indicated that CibZIP38, CibZIP55, and CibZIP43 are all nuclear-localized transcriptional activators. The report of the pecan bZIP gene family in this work can further improve our understanding of CibZIPs as a genetic resource for the genetic engineering breeding of pecan.

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Data availability

Genomic information of Carya illinoinensis was obtained from (GIGA)nDB (http://gigadb.org/) and the identified gene IDs are available in Table 1 of the article. A. thaliana genomes were obtained from the TAIR (https://www.arabidopsis.org/index.jsp). The genome sequence of C. paliurus was downloaded from Genome Warehouse in the National Genomics Data Center Beijing Institute of Genomics, Chinese Academy of Sciences/China National Center for Bioinformation (https://ngdc.cncb.ac.cn/gwh). Walnut whole genome data were downloaded from the NCBI database (http://www.ncbi.nlm.nih.gov/). Grape cds and protein sequences were downloaded from (http://genomes.cribi.unipd.it/). And all primer sequences can be found in the Appendix.

References

  • Aisala H, Manninen H, Laaksonen T, Linderborg KM, Myoda T, Hopia A, Sandell M (2020) Linking volatile and non-volatile compounds to sensory profiles and consumer liking of wild edible Nordic mushrooms. Food Chem 304

  • Azeem F, Tahir H, Ijaz U, Shaheen T (2020) A genome-wide comparative analysis of bZIP transcription factors in G. arboreum and G. raimondii (Diploid ancestors of present-day cotton). Physiol Mol Biol Plants 26:433–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. Plos One 9

  • Cantalapiedra CP, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829

    Article  CAS  PubMed  PubMed Central  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. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Choi J-W, Kim H-E, Kim S (2022) Two different domain architectures generate structural and functional diversity among bZIP genes in the Solanaceae family. Front Plant Sci 13:967546

    Article  PubMed  PubMed Central  Google Scholar 

  • Droege-Laser W, Snoek BL, Snel B, Weiste C (2018) The Arabidopsis bZIP transcription factor family - an update. Curr Opin Plant Biol 45:36–49

    Article  CAS  Google Scholar 

  • Duvaud S, Gabella C, Lisacek F, Stockinger H, Ioannidis V, Durinx C (2021) Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Res 49:W216–W227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, Vicente-Carbajosa J, Droege-Laser W (2006) Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46:890–900

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Wang Y, Zhang G, Gan Z, Gao M, Lv J, Wu T, Zhang X, Xu X, Yang S et al (2021) Group-C/S1 bZIP heterodimers regulate MdIPT5b to negatively modulate drought tolerance in apple species. Plant J 107:399–417

    Article  CAS  PubMed  Google Scholar 

  • Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  • Gai W-X, Ma X, Qiao Y-M, Shi B-H, ul Haq S, Li Q-H, Wei A-M, Liu K-K, Gong Z-H (2020) Characterization of the bZIP transcription factor family in pepper (Capsicum annuum L.): CabZIP25 positively modulates the salt tolerance. Front Plant Sci 11

  • Gao J, Wang M-J, Wang J-J, Lu H-P, Liu J-X (2022) bZIP17 regulates heat stress tolerance at reproductive stage in Arabidopsis. aBIOTECH3 :1–11

  • Gibalova A, Steinbachova L, Hafidh S, Blahova V, Gadiou Z, Michailidis C, Muller K, Pleskot R, Dupl’akova N, Honys D (2017) Characterization of pollen-expressed bZIP protein interactions and the role of ATbZIP18 in the male gametophyte. Plant Reproduction 30:1–17

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Huang R, Huang Y, Sun Z, Huang J, Wang Z (2017) Transcriptome analysis of genes involved in lipid biosynthesis in the developing embryo of pecan (Carya illinoinensis). J Agric Food Chem

  • Jagadish SVK, Way DA, Sharkey TD (2021) Plant heat stress: concepts directing future research. Plant, Cell Environ 44:1992–2005

    Article  CAS  PubMed  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Li M, Luo H, Zhai M, Guo Z, Li Y, Qiao Y, Wang L (2018) Transcriptome survey reveals candidate genes involved in lipid metabolism of Carya illinoinensis. Int J Agric Biol 20:991–1004

    CAS  Google Scholar 

  • Jia Z, Wang G, Xuan J, Zhang J, Zhai M, Jia X, Guo Z, Li M (2018) Comparative transcriptome analysis of pecan female and male inflorescences. Russ J Plant Physiol 65:186–196

    Article  CAS  Google Scholar 

  • Jin Z, Xu W, Liu A (2014) Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta 239:299–312

    Article  CAS  PubMed  Google Scholar 

  • Kang C, Zhai H, He S, Zhao N, Liu Q (2019) A novel sweetpotato bZIP transcription factor gene, IbbZIP1, is involved in salt and drought tolerance in transgenic Arabidopsis. Plant Cell Rep 38:1373–1382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Liu Y, Zhang X, Zhao B, Childs KL (2016) Analysis of salt-induced physiological and proline changes in 46 switchgrass (Panicum virgatum) lines indicates multiple response modes. Plant Physiol Biochem 105:203–212

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lara P, Onate-Sanchez L, Abraham Z, Ferrandiz C, Diaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Research MJNA (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P, Zheng T, Li L, Wang J, Cheng T, Zhang Q (2022) Genome-wide investigation of the bZIP transcription factor gene family in Prunus mume: classification, evolution, expression profile and low-temperature stress responses. Horticultural Plant Journal 8:230–242

    Article  CAS  Google Scholar 

  • Li D, Fu F, Zhang H, Song F (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics 16

  • Li Y-Y, Meng D, Li M, Cheng L (2016) Genome-wide identification and expression analysis of the bZIP gene family in apple (Malus domestica). Tree Genet Genomes 12

  • Liao Y, Zou H-F, Wei W, Hao Y-J, Tian A-G, Huang J, Liu Y-F, Zhang J-S, Chen S-Y (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240

    Article  CAS  PubMed  Google Scholar 

  • Liu JY (2003) Real-time PCR technique and its application in quantification of plant nucleic acid molecules. Acta Botanica Sinica 45:631–637

    CAS  Google Scholar 

  • Liu C, Mao B, Ou S, Wang W, Liu L, Wu Y, Chu C, Wang X (2018) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice (vol 84, pg 19, 2014). Plant Mol Biol 97:467–468

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Chen N, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng Z-M (2014). Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15

  • Liu H, Gao Y, Wang L, Lan Y, Wu M, Yan H, Xiang Y (2022) Identification and expression analysis of AP2/ERF superfamily in pecan (Carya illinoensis). Scientia Horticulturae 303

  • Ma H, Liu C, Li Z, Ran Q, Xie G, Wang B, Fang S, Chu J, Zhang J (2018) ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol 178:753–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manzoor MA, Manzoor MM, Li G, Abdullah M, Wang H, Han W, Shakoor A, Riaz MW, Rehman S, Cai Y (2021) Genome-wide identification and characterization of bZIP transcription factors and their expression profile under abiotic stresses in Chinese pear (Pyrus bretschneideri). BMC Plant Biol 21

  • Moon S-J, Han S-Y, Kim D-Y, Yoon IS, Shin D, Byun M-O, Kwon H-B, Kim B-G (2015) Ectopic expression of a hot pepper bZIP-like transcription factor in potato enhances drought tolerance without decreasing tuber yield. Plant Mol Biol 89:421–431

    Article  CAS  PubMed  Google Scholar 

  • Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Barrell D, Bateman A, Binns D, Biswas M, Bradley P, Bork P et al (2003) The InterPro Database, 2003 brings increased coverage and new features. Nucleic Acids Res 31:315–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ngangyo Heya M, Romo Hernandez AL, Foroughbakhch Pournavab R, Ibarra Pintor LF, Diaz-Jimenez L, Heya MS, Cruz LRS, Parra AC (2022) Physicochemical characteristics of biofuel briquettes made from pecan (Carya illinoensis) pericarp wastes of different particle sizes. Molecules 27

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan C, Zhang H, Ma Q, Fan F, Fu R, Ahammed GJ, Yu J, Shi K (2019) Role of ethylene biosynthesis and signaling in elevated CO2-induced heat stress response in tomato. Planta 250:563–572

    Article  CAS  PubMed  Google Scholar 

  • Pan G, Sun C, Liao Z, Tang J (2021) Machine and deep learning for prediction of subcellular localization. Methods in Molecular Biology (clifton, NJ) 2361:249–261

    Article  CAS  Google Scholar 

  • Pan F, Wu M, Hu W, Liu R, Yan H, Xiang Y (2019) Genome-wide identification and expression analyses of the bZIP transcription factor genes in moso bamboo (Phyllostachys edulis). Int J Mol Sci 20

  • Perez-Rodriguez P, Riano-Pachon DM, Correa LGG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PInTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827

    Article  CAS  PubMed  Google Scholar 

  • Polozola ME II, Wells DE, Foshee WG, Kessler JR, Wright AN (2017) Effects of phosphorus rate on pecan Carya illinoinensis (Wangenh.) K. Koch Seedling Development Hortscience 52:S45–S45

    Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  • Sagor GHM, Berberich T, Tanaka S, Nishiyama M, Kanayama Y, Kojima S, Muramoto K, Kusano T (2016) A novel strategy to produce sweeter tomato fruits with high sugar contents by fruit-specific expression of a single bZIP transcription factor gene. Plant Biotechnol J 14:1116–1126

    Article  CAS  PubMed  Google Scholar 

  • Schwechheimer C, Zourelidou M, Bevan MW (1998) Plant transcription factor studieS. Annu Rev Plant Physiol Plant Mol Biol 49:127–150

    Article  CAS  PubMed  Google Scholar 

  • Song Z, Wang L, Lai C, Lee M, Yang Z, Yue G (2022) EgSPEECHLESS Responses to salt stress by regulating stomatal development in oil palm. Int J Mol Sci 23

  • Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P et al (2021) The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets (vol 49, pg D605, 2021). Nucleic Acids Res 49:10800–10800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao Y-T, Chen L-X, Jin J, Du Z-K, Li J-M (2022) Genome-wide identification and analysis of bZIP gene family reveal their roles during development and drought stress in Wheel Wingnut (Cyclocarya paliurus). BMC Genomics 23

  • Venkatachalam M, Kshirsagar HH, Seeram NP, Heber D, Thompson TE, Roux KH, Sathe SK (2007) Biochemical composition and immunological comparison of select pecan Carya illinoinensis (Wangenh.) K. Koch cultivars. J Agric Food Chem 55:9899–9907

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Cheng K, Wan L, Yan L, Jiang H, Liu S, Lei Y, Liao B (2015) Genome-wide analysis of the basic leucine zipper (bZIP) transcription factor gene family in six legume genomes. BMC Genomics 16

  • Wang X-L, Chen X, Yang T-B, Cheng Q, Cheng Z-M (2017) Genome-wide identification of bZIP family genes involved in drought and heat stresses in strawberry (Fragaria vesca). Int J Genomics 2017

  • Wang D, Meng S, Su W, Bao Y, Lu Y, Yin W, Liu C, Xia X (2019) Genome-wide analysis of multiple organellar RNA editing factor family in poplar reveals evolution and roles in drought stress. Int J Mol Sci 20

  • Wang L, Chen F, Lan Y, Liu H, Wu M, Yan H, Xiang Y (2023) Genome-wide identification of B3 superfamily in pecan (Carya illinoensis): in silico and experimental analyses. Sci Hortic 307

  • Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Z, Liang J, Wang C, Zhao X, Zhong X, Cao X, Li G, He J, Yi M (2018) Overexpression of lily HsfA3s in Arabidopsis confers increased thermotolerance and salt sensitivity via alterations in proline catabolism. J Exp Bot 69:2005–2021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing S, Chen K, Zhu H, Zhang R, Zhang H, Li B, Gao C (2020) Fine-tuning sugar content in strawberry. Genome Biology 21

  • Xing H, Jiang Y, Zou Y, Long X, Wu X, Ren Y, Li Y, Li H-L (2021) Genome-wide investigation of the AP2/ERF gene family in ginger: evolution and expression profiling during development and abiotic stresses. BMC Plant Biology 21

  • Xu Q, He H, He B, Li T, Liu Y, Zhu S, Zhang G (2022) Nitrogen allocation tradeoffs within-leaf between photosynthesis and high-temperature adaptation among different varieties of pecan (Carya illinoinensis Wangenh. K. Koch). Plants-Basel 11

  • Yang Q-Q, Feng K, Xu Z-S, Duan A-Q, Liu J-X, Xiong A-S (2019) Genome-wide identification of bZIP transcription factors and their responses to abiotic stress in celery. Biotechnol Biotechnol Equip 33:707–718

    Article  CAS  Google Scholar 

  • Zhang Z, Quan S, Niu J, Guo C, Kang C, Liu J, Yuan X (2022) Genome-wide identification, classification, expression and duplication analysis of bZIP family genes in Juglans regia L. Int J Mol Sci 23

  • Zhao F, Zhang D, Zhao Y, Wang W, Yang H, Tai F, Li C, Hu X (2016) The difference of physiological and proteomic changes in maize leaves adaptation to drought, heat, and combined both stresses. Front Plant Sci 7

  • Zhao K, Chen S, Yao W, Cheng Z, Zhou B, Jiang T (2021) Genome-wide analysis and expression profile of the bZIP gene family in poplar. BMC Plant Biol 21

  • Zhou Y, Xu D, Jia L, Huang X, Ma G, Wang S, Zhu M, Zhang A, Guan M, Lu K, et al (2017) Genome-wide identification and structural analysis of bZIP transcription factor genes in Brassica napus. Genes8

  • Zhou L, Yarra R (2022) Genome-wide identification and expression analysis of bZIP transcription factors in oil palm (Elaeis guineensis Jacq.) under abiotic stress. Protoplasma 259:469–483

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Meng X, Cai J, Li G, Dong T, Li Z (2018) Basic leucine zipper transcription factor SIbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biol 18

  • Zhu K, Fan P, Mo Z, Tan P, Feng G, Li F, Peng F (2020) Identification, expression and co-expression analysis of R2R3-MYB family genes Involved in graft union formation in pecan (Carya illinoinensis). Forests 11

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Acknowledgements

We thank the members of Anhui Provincial Key Laboratory of Forest Resources and Silviculture for their assistance in this study.

Funding

This work was supported by the Key Project of Scientific Research of Anhui Provincial Education Department (Grant no. 2022AH050903).

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NQJ designed and conducted the experiments, wrote the manuscript, and processed the figures. XYZ and WH assisted with part of the experiment. LNW and YGL helped to handle figures and tables. HWY and MW helped to revise the manuscript. YX provided financial support for the article and designed the way and frame of this study. All the authors read and approved the final manuscript.

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Correspondence to Yan Xiang.

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Jiang, N., Wang, L., Lan, Y. et al. Genome-wide identification of the Carya illinoinensis bZIP transcription factor and the potential function of S1-bZIPs in abiotic stresses. Tree Genetics & Genomes 19, 47 (2023). https://doi.org/10.1007/s11295-023-01622-w

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