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Genomewide analysis of homeobox gene family in apple (Malus domestica Borkh.) and their response to abiotic stress

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Abstract

Homeobox proteins (HOXs) comprise a large family in eukaryotes and share a highly conserved DNA-binding motif, the homeodomain (HD). HOXs play an important role in the regulation of plant growth, development and stress response. However, systematic analysis and expression profiling of these genes have not been reported in Malus domestica. In this study, a total of 207 HOXs of M. domestica (MdHOXs) were identified and classified into 11 distinct subfamilies, and an unclassified group according to their functional domains. The MdHOXs were localized in all 17 chromosomes with various densities and a majority of them tended to form gene clusters. Analysis of the \(K_{\mathrm{a}}/K_{\mathrm{s}}\) ratios suggested that the duplicated genes of MdHOXs mainly underwent purifying selection with restrictive functional divergence after the duplication events. The expression of MdHOXs has organ specific characteristics and were divided into seven different groups. Stress-related cis-acting elements were prevalent in the upstream sequence of MdHOXs by systematic analysis. To explore the response to abiotic stress, eight MdHOXs were randomly selected to investigate their expression using quantitative real-time polymerase chain reaction. Transcription levels of MdHOXs were upregulated in the leaves and roots under cold, osmotic, high salinity or exogenous ABA treatments, which suggested that they may take part in the plant response to abiotic stress. These results provided basic information of HOXs in apple and will further contribute to the functional research of MdHOXs, especially the response to abiotic stress.

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References

  • Angela H. and Miltos T. 2010 KNOX genes: versatile regulators of plant development and diversity. Development 137, 3153–3165.

    Article  Google Scholar 

  • Ariel F. D., Manavella P. A., Dezar C. A. and Chan R. L. 2007 The true story of the HD-Zip family. Trends Plant Sci. 12, 419–426.

    Article  CAS  Google Scholar 

  • Bhattacharjee A., Ghangal R., Garg R. and Jain M. 2015 Genome-wide analysis of homeobox gene family in legumes: identification, gene duplication and expression profiling. PLoS One 10, e0119198.

    Article  Google Scholar 

  • Burglin T. R. and Affolter M. 2016 Homeodomain proteins: an update. Chromosoma 125, 497–521.

    Article  CAS  Google Scholar 

  • Chan R. L., Gago G. M., Palena C. M. et al. 1998 Homeoboxes in plant development. Biochim. Biophys. Acta 1442, 1–19.

    Article  CAS  Google Scholar 

  • Chen X., Chen Z., Zhao H., Zhao Y., Cheng B. and Xiang Y. 2014 Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PLoS One 9, e87156.

    Article  Google Scholar 

  • Cheng S., Huang Y., Zhu N. and Zhao Y. 2014 The rice WUSCHEL-related homeobox genes are involved in reproductive organ development, hormone signaling and abiotic stress response. Gene 549, 266–274.

    Article  CAS  Google Scholar 

  • Costanzo E., Trehin C. and Vandenbussche M. 2014 The role of WOX genes in flower development. Ann. Bot. 114, 1545–1553.

    Article  CAS  Google Scholar 

  • Cui H. R., Zhang Z. R., Lv W., Xu J. N. and Wang X. Y. 2015 Genome-wide characterization and analysis of F-box protein-encoding genes in the Malus domestica genome. Mol. Genet. Genomics 290, 1435–1446.

    Article  CAS  Google Scholar 

  • Dong Y. H., Yao J. L., Atkinson R. G., Putterill J. J., Morris B. A. and Gardner R. C. 2000 MDH1 an apple homeobox gene belonging to the BEL1 family. Plant Mol. Biol. 9, 42–49.

    Google Scholar 

  • Du D., Zhang Q., Cheng T., Pan H., Yang W. and Sun L. 2013 Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume. Mol. Biol. Rep. 40, 1937–1946.

    Article  Google Scholar 

  • Eddy S. R. 1998 Profile hidden Markov models. Bioinformatics 14, 78–96.

    Article  Google Scholar 

  • Gasic K., Hernandez A. and Korban S. S. 2004 RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol. Biol. Rep. 22, 437–444.

    Article  CAS  Google Scholar 

  • Hake S. 2016 Homeobox gene in the functioning of plant meristem. Biol. Sci. 350, 45–51.

    Google Scholar 

  • Higo K., Ugawa Y., Iwamoto M. and Higo H. 1998 Place: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res. 26, 358–359.

    Article  CAS  Google Scholar 

  • Hu R., Chi X., Chai G., Kong Y., He G., Wang X. et al. 2012 Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One 7, e31149.

    Article  CAS  Google Scholar 

  • Jain M., Tyagi A. K. and Khurana J. P. 2008 Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J. 275, 2845–2861.

    Article  CAS  Google Scholar 

  • Katiyar S., Till E. A. and Lennarz W. J. 2001 Studies on the function of yeast protein disulfide isomerase in renaturation of proteins. Biochim. Biophys. Acta 15, 22–31.

    Google Scholar 

  • Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H. et al. 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.

    Article  CAS  Google Scholar 

  • Li Y., Wu B., Yu Y., Yang G., Wu C. and Zheng C. 2011 Genome-wide analysis of the RING finger gene family in apple. Mol. Genet. Genomics 286, 81–94.

    Article  CAS  Google Scholar 

  • Liu W., Fu R., Li Q., Li J., Wang L. and Ren Z. 2013 Genome-wide identification and expression profile of homeodomain-leucine zipper Class I gene family in Cucumis sativus. Gene 531, 279–287.

    Article  CAS  Google Scholar 

  • Liu X., Li R., Dai Y., Chen, X. and Wang X. 2017 Genome-wide identification and expression analysis of the B-box gene family in the Apple (Malus domestica Borkh.) genome. Mol. Genet. Genomics 293, 303–315.

    Article  Google Scholar 

  • Maeda R. K. and Karch F. 2015 The open for business model of the bithorax complex in Drosophila. Chromosoma 124, 293–307.

    Article  CAS  Google Scholar 

  • Mukherjee K., Brocchieri L. and Burglin T. R. 2009 A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol. Biol. Evol. 26, 2775–2794.

    Article  CAS  Google Scholar 

  • Quraishi U. M., Abrouk M., Murat F., Pont C., Foucrier S., Desmaizieres G. et al. 2011 Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J. 65, 745–756.

    Article  CAS  Google Scholar 

  • Sharma P., Lin T., Grandellis C., Yu M. and Hannapel D. J. 2014 The BEL1-like family of transcription factors in potato. J. Exp. Bot. 65, 709–723.

    Article  CAS  Google Scholar 

  • Shu Y., Liu Y., Zhang J., Song L. and Guo C. 2015 Genome-wide analysis of the AP2/ERF superfamily genes and their responses to Abiotic stress in Medicago truncatula. Front. Plant Sci. 6, 12–47.

  • Shu Y., Tao Y., Wang S., Huang L., Yu X., Wang Z. et al. 2015 GmSBH1, a homeobox transcription factor gene, relates to growth and development and involves in response to high temperature and humidity stress in soybean. Plant Cell Rep. 34, 1927–1937.

    Article  CAS  Google Scholar 

  • Tan Q. K. and Irish V. F. 2006 The Arabidopsis zinc finger-homeodomain genes encode proteins with unique biochemical properties that are coordinately expressed during floral development. Plant Physiol. 140, 1095–1108.

    Article  CAS  Google Scholar 

  • Tsuda K., Kurata N., Ohyanagi H. and Hake S. 2014 Genome-wide study of KNOX regulatory network reveals brassinosteroid catabolic genes important for shoot meristem function in rice. Plant Cell 26, 3488–3500.

    Article  CAS  Google Scholar 

  • Velasco R., Zharkikh A., Affourtit J., Dhingra A., Cestaro A., Kalyanaraman A. et al. 2010 The genome of the domesticated apple (Malus\(\times \)domestica Borkh.). Nat. Genet. 42, 833–839.

    Article  CAS  Google Scholar 

  • Wang X. L., Zhong Y., Cheng Z. M. and Xiong J. S. 2015 Divergence of the bZIP gene family in strawberry, peach, and apple suggests multiple modes of gene evolution after duplication. Int. J. Genomics 536, 39–43.

    Google Scholar 

  • Wu S., Wu M., Dong Q., Jiang H., Cai R. and Xiang Y. 2016 Genome-wide identification, classification and expression analysis of the PHD-finger protein family in Populus trichocarpa. Gene 575, 75–89.

    Article  CAS  Google Scholar 

  • Xu J. N., Xing S. S., Zhang Z. R., Chen X. S. and Wang X. Y. 2016 Genome-wide identification and expression analysis of the Tubby-like protein family in the Malus domestica genome. Front. Plant Sci. 7, 64–69.

  • Xu J. N., Xing S. S., Cui H. R., Chen X. S. and Wang X. Y. 2016 Genome-wide identification and characterization of the apple (Malus domestica) HECT ubiquitin-protein ligase family and expression analysis of their responsiveness to abiotic stresses. Mol. Genet. Genomics 291, 635–646.

    Article  Google Scholar 

  • Zhao T., Liang D., Wang P., Liu J. and Ma F. 2012 Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol. Genet. Genomics 287, 423–436.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Special Research Fund of Public Welfare of China Agricultural Ministry (201303093) and China Natural Foundation (31872042).

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Authors and Affiliations

  1. College of Life Science, State Key Laboratory of Crop Biology, Shandong Agricultural University, Taian,  271018, Shandong, People’s Republic of China

    Rong Li, Yaqing Dai, Li Yuan, Xin Liu, Qinghua Sun & Xiaoyun Wang

  2. Qingdao Academy of Agricultural Science, Qingdao,  266100, Shandong, People’s Republic of China

    Hongjuan Ge

Authors
  1. Rong Li
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  2. Hongjuan Ge
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  3. Yaqing Dai
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  4. Li Yuan
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  5. Xin Liu
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  6. Qinghua Sun
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  7. Xiaoyun Wang
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Corresponding authors

Correspondence to Qinghua Sun or Xiaoyun Wang.

Additional information

Corresponding editor: U. C. Lavania

Qinghua Sun and Rong Li conceived and designed this research; Rong Li, Xin Liu, Li Yuan and Yaqing Dai performed the experiments; Rong Li, Qinghua Sun and Hongjuan Ge analysed the data and Xiaoyun Wang, Qinghua Sun and Rong Li wrote the paper. All authors read and approved the manuscript.

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Li, R., Ge, H., Dai, Y. et al. Genomewide analysis of homeobox gene family in apple (Malus domestica Borkh.) and their response to abiotic stress. J Genet 98, 13 (2019). https://doi.org/10.1007/s12041-018-1049-y

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  • DOI: https://doi.org/10.1007/s12041-018-1049-y

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