Abstract
Main conclusion
Genome-wide identification revealed 79 BpNAC genes belonging to 16 subfamilies, and their gene structures and evolutionary relationships were characterized. Expression analysis highlighted their importance in plant selenium stress responses.
Abstract
Paper mulberry (Broussonetia papyrifera), a deciduous arboreal plant of the Moraceae family, is distinguished by its leaves, which are abundant in proteins, polysaccharides, and flavonoids, positioning it as a novel feedstock. NAC transcription factors, exclusive to plant species, are crucial in regulating growth, development, and response to biotic and abiotic stress. However, extensive characterization of the NAC family within paper mulberry is lacking. In this study, 79 BpNAC genes were identified from the paper mulberry genome, with an uneven distribution across 13 chromosomes. A comprehensive, genome-wide analysis of BpNACs was performed, including investigating gene structures, promoter regions, and chromosomal locations. Phylogenetic tree analysis, alongside comparisons with Arabidopsis thaliana NACs, allowed for categorizing these genes into 16 subfamilies in alignment with gene structure and motif conservation. Collinearity analysis suggested a significant homologous relationship between the NAC genes of paper mulberry and those in Morus notabilis, Ficus hispida, Antiaris toxicaria, and Cannabis sativa. Integrating transcriptome data and Se content revealed that 12 BpNAC genes were associated with selenium biosynthesis. Subsequent RT-qPCR analysis corroborated the correlation between BpNAC59, BpNAC62 with sodium selenate, and BpNAC55 with sodium selenite. Subcellular localization experiments revealed the nuclear functions of BpNAC59 and BpNAC62. This study highlights the potential BpNAC transcription factors involved in selenium metabolism, providing a foundation for strategically breeding selenium-fortified paper mulberry.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
An JP, Yao JF, Xu RR et al (2018) An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant 164:279–289. https://doi.org/10.1111/ppl.12724
An X, Zhang S, Li T et al (2021) Transcriptomics analysis reveals the effect of Broussonetia papyrifera L. fermented feed on meat quality traits in fattening lamb. PeerJ 9:e11295. https://doi.org/10.7717/peerj.11295
Avery JC, Hoffmann PR (2018) Selenium, selenoproteins, and immunity. Nutrients 10:1203. https://doi.org/10.3390/nu10091203
Baranwal VK, Khurana P (2016) Genome-wide analysis, expression dynamics and varietal comparison of NAC gene family at various developmental stages in Morus notabilis. Mol Genet Genomics MGG 291:1305–1317. https://doi.org/10.1007/s00438-016-1186-z
Çakır Ö, Turgut-Kara N, Arı Ş, Zhang B (2015) De novo transcriptome assembly and comparative analysis elucidate complicated mechanism regulating astragalus chrysochlorus response to selenium stimuli. PLoS ONE 10:e0135677. https://doi.org/10.1371/journal.pone.0135677
Cao D, Liu Y, Ma L et al (2018) Transcriptome analysis of differentially expressed genes involved in selenium accumulation in tea plant (Camellia sinensis). PLoS ONE 13:e0197506. https://doi.org/10.1371/journal.pone.0197506
Chen Q, Yu L, Chao W et al (2022) Comparative physiological and transcriptome analysis reveals the potential mechanism of selenium accumulation and tolerance to selenate toxicity of Broussonetia papyrifera. Tree Physiol 42:2578–2595. https://doi.org/10.1093/treephys/tpac095
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
Chen Q, Zhu C, Guo L et al (2024) Genome wide identification of HMT gene family explores BpHMT2 enhancing the selenium accumulation and tolerance in Broussonetia papyrifera. Tree Physiol. https://doi.org/10.1093/treephys/tpae030
Duarte JM, Cui L, Wall PK et al (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23:469–478. https://doi.org/10.1093/molbev/msj051
El Mehdawi AF, Cappa JJ, Fakra SC et al (2012) Interactions of selenium hyperaccumulators and nonaccumulators during cocultivation on seleniferous or nonseleniferous soil-the importance of having good neighbors. New Phytol 194:264–277. https://doi.org/10.1111/j.1469-8137.2011.04043.x
Gu C, Shang L, Zhang G et al (2022) Identification and expression analysis of NAC gene family in weeping trait of Lagerstroemia indica. Plants Basel Switz 11:2168. https://doi.org/10.3390/plants11162168
Han K, Zhao Y, Sun Y, Li Y (2023) NACs, generalist in plant life. Plant Biotechnol J. https://doi.org/10.1111/pbi.14161
Hu R, Qi G, Kong Y et al (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145. https://doi.org/10.1186/1471-2229-10-145
Hussey SG, Saïdi MN, Hefer CA et al (2015) Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol 206:1337–1350. https://doi.org/10.1111/nph.13139
Javed T, Shabbir R, Ali A et al (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants Basel Switz 9:491. https://doi.org/10.3390/plants9040491
Jia D, Jiang Z, Fu H et al (2021) Genome-wide identification and comprehensive analysis of NAC family genes involved in fruit development in kiwifruit (Actinidia). BMC Plant Biol 21:44. https://doi.org/10.1186/s12870-020-02798-2
Jiang L, Yang J et al (2020) Overexpression of ethylene response factor ERF96 gene enhances selenium tolerance in Arabidopsis. Plant Physiol Biochem: PPB 149:294–300. https://doi.org/10.1016/j.plaphy.2020.02.024
Kapoor B, Kumar P, Gill NS et al (2023) Molecular mechanisms underpinning the silicon-selenium (Si-Se) interactome and cross-talk in stress-induced plant responses. Plant Soil 486:45–68. https://doi.org/10.1007/s11104-022-05482-6
Khattab HI, Emam MA, Emam MM et al (2014) Effect of selenium and silicon on transcription factors NAC5 and DREB2A involved in drought-responsive gene expression in rice. Biol Plant 58:265–273. https://doi.org/10.1007/s10535-014-0391-z
Konasani VR, Kadre S (2015) Correlation and linear regression. In: Konasani VR, Kadre S (eds) Practical business analytics using SAS: a hands-on guide. Apress, Berkeley, CA, pp 295–349
Lallemand T, Leduc M, Landès C et al (2020) An overview of duplicated gene detection methods: why the duplication mechanism has to be accounted for in their choice. Genes 11:1046. https://doi.org/10.3390/genes11091046
Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296. https://doi.org/10.1093/nar/gkab301
Li X, Li X, Li M et al (2016) Dual function of NAC072 in ABF3-mediated ABA-responsive gene regulation in Arabidopsis. Front Plant Sci 7:1075. https://doi.org/10.3389/fpls.2016.01075
Li C, Zhang J, Zhang Q et al (2022a) Genome-wide identification and analysis of the NAC transcription factor gene family in Garden Asparagus (Asparagus officinalis). Genes 13:976. https://doi.org/10.3390/genes13060976
Li M, Fan X, Cheng Q et al (2022b) Effect of amomum villosum essential oil as an additive on the chemical composition, fermentation quality, and bacterial community of paper mulberry silage. Front Microbiol 13:951958. https://doi.org/10.3389/fmicb.2022.951958
Li Y, Han H, Fu M et al (2023) Genome-wide identification and expression analysis of NAC family genes in Ginkgo biloba L. Plant Biol Stuttg Ger 25:107–118. https://doi.org/10.1111/plb.13486
Liu M, Ma Z, Sun W et al (2019) Genome-wide analysis of the NAC transcription factor family in Tartary buckwheat (Fagopyrum tataricum). BMC Genom 20:113. https://doi.org/10.1186/s12864-019-5500-0
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
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. https://doi.org/10.1126/science.290.5494.1151
Mao H, Li S, Chen B et al (2022) Variation in cis-regulation of a NAC transcription factor contributes to drought tolerance in wheat. Mol Plant 15:276–292. https://doi.org/10.1016/j.molp.2021.11.007
Meng X, Liu S, Zhang C et al (2023) The unique sweet potato NAC transcription factor IbNAC3 modulates combined salt and drought stresses. Plant Physiol 191:747–771. https://doi.org/10.1093/plphys/kiac508
Narusaka Y, Nakashima K, Shinwari ZK et al (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148. https://doi.org/10.1046/j.1365-313X.2003.01708.x
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Nuruzzaman M, Manimekalai R, Sharoni AM et al (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44. https://doi.org/10.1016/j.gene.2010.06.008
Ooka H, Satoh K, Doi K et al (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res Int J Rapid Publ Rep Genes Genomes 10:239–247. https://doi.org/10.1093/dnares/10.6.239
Peng X, Yucheng W, Ruiping H et al (2014) Global transcriptomics identification and analysis of transcriptional factors in different tissues of the paper mulberry. BMC Plant Biol 14:194. https://doi.org/10.1186/s12870-014-0194-6
Peng X, Liu H, Chen P et al (2019) A chromosome-scale genome assembly of paper mulberry (Broussonetia papyrifera) provides new insights into its forage and papermaking usage. Mol Plant 12:661–677. https://doi.org/10.1016/j.molp.2019.01.021
Peng H, Phung J, Zhai Y, Neff MM (2020) Self-transcriptional repression of the Arabidopsis NAC transcription factor ATAF2 and its genetic interaction with phytochrome A in modulating seedling photomorphogenesis. Planta 252:48. https://doi.org/10.1007/s00425-020-03456-5
Prabhu KS, Lei XG (2016) Selenium12. Adv Nutr 7:415–417. https://doi.org/10.3945/an.115.010785
Pu Z, Wei G et al (2021) Selenium and anthocyanins share the same transcription factors R2R3MYB and bHLH in wheat. Food Chem 356:129699. https://doi.org/10.1016/j.foodchem.2021.129699
Qiao X, Li Q, Yin H et al (2019) Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol 20:38. https://doi.org/10.1186/s13059-019-1650-2
Reams AB, Roth JR (2015) Mechanisms of gene duplication and amplification. Cold Spring Harb Perspect Biol 7:a016592. https://doi.org/10.1101/cshperspect.a016592
Sakuraba Y, Bülbül S, Piao W et al (2017) Arabidopsis EARLY FLOWERING3 increases salt tolerance by suppressing salt stress response pathways. Plant J Cell Mol Biol 92:1106–1120. https://doi.org/10.1111/tpj.13747
Shang X, Yu Y, Zhu L et al (2020) A cotton NAC transcription factor GhirNAC2 plays positive roles in drought tolerance via regulating ABA biosynthesis. Plant Sci Int J Exp Plant Biol 296:110498. https://doi.org/10.1016/j.plantsci.2020.110498
Shen S, Zhang Q, Shi Y et al (2019) Genome-wide analysis of the NAC domain transcription factor gene family in Theobroma cacao. Genes 11:35. https://doi.org/10.3390/genes11010035
Si B, Tao H, Zhang X et al (2018) Effect of Broussonetia papyrifera L. (paper mulberry) silage on dry matter intake, milk composition, antioxidant capacity and milk fatty acid profile in dairy cows. Asian-Australas J Anim Sci 31:1259–1266. https://doi.org/10.5713/ajas.17.0847
Souer E, van Houwelingen A, Kloos D et al (1996) The No Apical Meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85:159–170. https://doi.org/10.1016/S0092-8674(00)81093-4
Su H, Zhang S, Yuan X et al (2013) Genome-wide analysis and identification of stress-responsive genes of the NAM-ATAF1,2-CUC2 transcription factor family in apple. Plant Physiol Biochem 71:11–21. https://doi.org/10.1016/j.plaphy.2013.06.022
Sukiran NL, Ma JC, Ma H, Su Z (2019) ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis. Plant Mol Biol 99:161–174. https://doi.org/10.1007/s11103-018-0810-1
Sun W, Cao Z, Li Y et al (2007) A simple and effective method for protein subcellular localization using Agrobacterium-mediated transformation of onion epidermal cells. Biologia (bratisl) 62:529–532. https://doi.org/10.2478/s11756-007-0104-6IF:1.5Q3
Sun L, Zhang P, Wang R et al (2019a) The SNAC-A transcription factor ANAC032 reprograms metabolism in Arabidopsis. Plant Cell Physiol 60:999–1010. https://doi.org/10.1093/pcp/pcz015
Sun Q, Jiang S, Zhang T et al (2019b) Apple NAC transcription factor MdNAC52 regulates biosynthesis of anthocyanin and proanthocyanidin through MdMYB9 and MdMYB11. Plant Sci 289:110286. https://doi.org/10.1016/j.plantsci.2019.110286
Tao H, Si B, Xu W et al (2020) Effect of Broussonetia papyrifera L. silage on blood biochemical parameters, growth performance, meat amino acids and fatty acids compositions in beef cattle. Asian-Australas J Anim Sci 33:732–741. https://doi.org/10.5713/ajas.19.0150
Tognetti S, Speck C (2016) Replicating repetitive DNA. Nat Cell Biol 18:593–594. https://doi.org/10.1038/ncb3367
Trippe RC, Pilon-Smits EAH (2021) Selenium transport and metabolism in plants: phytoremediation and biofortification implications. J Hazard Mater 404:124178. https://doi.org/10.1016/j.jhazmat.2020.124178
Van Hoewyk D, Takahashi H, Inoue E et al (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253. https://doi.org/10.1111/j.1399-3054.2007.01002.x
Vizueta J, Sánchez-Gracia A, Rozas J (2020) bitacora: a comprehensive tool for the identification and annotation of gene families in genome assemblies. Mol Ecol Resour 20:1445–1452. https://doi.org/10.1111/1755-0998.13202
Wang N, Zheng Y, Xin H et al (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75. https://doi.org/10.1007/s00299-012-1340-y
Wang M, Ren LT, Wei XY et al (2022) NAC transcription factor TwNAC01 positively regulates drought stress responses in Arabidopsis and Triticale. Front Plant Sci 13:877016. https://doi.org/10.3389/fpls.2022.877016
Wu JS, Lee C, Wu CC, Shiue YL (2004) Primer design using genetic algorithm. Bioinformatics 20:1710–1717. https://doi.org/10.1093/bioinformatics/bth147
Wu X, Tao M, Meng Y et al (2020) The role of WRKY47 gene in regulating selenium tolerance in Arabidopsis thaliana. Plant Biotechnol Rep 14:121–129. https://doi.org/10.1007/s11816-019-00560-1
Xu B, Ohtani M, Yamaguchi M et al (2014) Contribution of NAC transcription factors to plant adaptation to land. Science 343:1505–1508. https://doi.org/10.1126/science.1248417
Yang C, Huang Y, Lv P et al (2022) NAC transcription factor GmNAC12 improved drought stress tolerance in soybean. Int J Mol Sci 23:12029. https://doi.org/10.3390/ijms231912029
Yu M, Liu J, Du B et al (2021) NAC transcription factor PwNAC11 activates ERD1 by interaction with ABF3 and DREB2A to enhance drought tolerance in transgenic Arabidopsis. Int J Mol Sci 22:6952. https://doi.org/10.3390/ijms22136952
Zhang H, Xu J, Chen H et al (2021) Characterization of NAC family genes in Salvia miltiorrhiza and NAC2 potentially involved in the biosynthesis of tanshinones. Phytochemistry 191:112932. https://doi.org/10.1016/j.phytochem.2021.112932
Zhong R, Lee C, Haghighat M, Ye Z-H (2021) Xylem vessel-specific SND5 and its homologs regulate secondary wall biosynthesis through activating secondary wall NAC binding elements. New Phytol 231:1496–1509. https://doi.org/10.1111/nph.17425
Zou J, Lin J, Zhang B et al (2022) An efficient propagation system through root cuttings of an ecological and economic value plant-Broussonetia papyrifera (L.) L’Hér. ex Vent. Plants 11:1423. https://doi.org/10.3390/plants11111423
Funding
This work was supported by the National Natural Science Foundation of China (No. 32371929), the Key Research and Development Program of Hubei Province, China (No. 2023BBB065), Hubei Key Laboratory of Selenium Resource Research and Biological Application (No. PT10202311), and Jingzhou City Science and Technology Plan (No. 2023EC40).
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Longfei Guo: software; visualization; writing—original draft. Yongling Liao: data curation; project administration; resources; supervision; writing—review and editing. Shiming Deng: software. Jitao Li: software. Xianchen Bu: visualization. Changye Zhu: software. Xin Cong: methodology; software. Shuiyuan Cheng: methodology. Weiwei Zhang: methodology. Qiangwen Chen: methodology, data curation, writing—review and editing. Feng Xu: project administration; visualization; writing—review and editing.
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Guo, L., Liao, Y., Deng, S. et al. Genome-wide analysis of NAC transcription factors and exploration of candidate genes regulating selenium metabolism in Broussonetia papyrifera. Planta 260, 1 (2024). https://doi.org/10.1007/s00425-024-04438-7
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DOI: https://doi.org/10.1007/s00425-024-04438-7