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Characterization and expression profile analysis of YABBY family genes in Pak-choi (Brassica rapa ssp. chinensis) under abiotic stresses and hormone treatments

  • Hualan Hou
  • Peng Wu
  • Liwei Gao
  • Changwei Zhang
  • Xilin HouEmail author
Original Paper
  • 65 Downloads

Abstract

YABBY proteins are widely distributed among different plant species and exhibit a higher degree of prevalence in angiosperms than in gymnosperms; abaxial cell fate in the lateral organs of plants is mainly determined by the functions of YABBY genes. However, to date, no scientific study has been conducted on the functions and responses of these genes under different forms of abiotic stresses in Pak-choi (Brassica rapa ssp. chinensis). In this study, we cloned and identified 12 YABBY family genes from Pak-choi. The evolutionary history of the YABBY genes was studied in nine species and showed that YABBY gene loss occurred during specific periods or in certain species during evolution. The putative YABBY family genes of Pak-choi were comprehensively analyzed by comparison with the corresponding orthologs in Arabidopsis and Chinese cabbage (Brassica rapa ssp. pekinensis) and classified into five subfamilies based on the specific protein domains and phylogenetic clades. A subcellular localization assay involving BcYABBY1b and BcYABBY2c confirmed that the BcYABBY proteins were localized in the nucleus. qRT-PCR data revealed that the BcYABBY genes are specifically expressed in distinct organs and developmental stages. Furthermore, the expression profiles of the BcYABBY genes were investigated under different hormone treatments and abiotic stress factors. In this study, we comprehensively identified and analyzed the YABBY gene family in the Pak-choi genome. Our data provide possible functional information regarding the involvement of BcYABBY genes in plant growth and development and in the response to abiotic stress and hormone treatments.

Keywords

YABBY Pak-choi Subcellular localization Abiotic stress Hormone Expression profile 

Notes

Acknowledgements

This work was supported by The National Key Research and Development Program of China (Grant No. 2016YFD0101701) and the Science and Technology Pillar Program of Jiangsu Province (Grant No. BE2013429).

Author contributions

H-LH and X-LH conceived the project. H-LH and PW retrieved the datasets from the databases and analyzed the data. H-LH carried out the gene cloning and qRT-PCR experiments. C-WZ provided advice on the manuscript. PW, L-WG and C-WZ revised and proofread the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

10725_2019_475_MOESM1_ESM.jpg (254 kb)
Supplementary Figure S1 Distribution ofBrYABBYgenes on 6 chromosomes. The 24 ancestral blocks and three subgenomes of Chinese cabbage were plotted, based on the Chinese cabbage genome sequencing analysis result and the size of each chromosome can be estimated by the scale on the left of the figure. The different colored bars represent different subgenomes (LF, MF1, and MF2) (JPG 254 KB)
10725_2019_475_MOESM2_ESM.jpg (830 kb)
Supplementary Figure S2 YABBY homologous genes in segmental syntenic regions of the genomes ofBrassica rapaandArabidopsis thaliana. The ten B. rapa chromosomes and the five A. thaliana chromosomes are shown on horizontal axis and vertical axis, respectively. Green dots indicate YABBY homologs in the two species (JPG 830 KB)
10725_2019_475_MOESM3_ESM.jpg (2.2 mb)
Supplementary Figure S3 Different motif LOGOs are indicated by different colors from 1 to 10 (JPG 2230 KB)
10725_2019_475_MOESM4_ESM.xls (22 kb)
Supplementary Table S1 Primers used for RT-PCR and qRT-PCR (XLS 22 KB)

References

  1. Bailey TL et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208CrossRefGoogle Scholar
  2. Bartley GE, Ishida BK (2002) Digital fruit ripening: data mining in the TIGR tomato gene index. Plant Mol Biol Rep 20:115–130CrossRefGoogle Scholar
  3. Bartley GE, Ishida BK (2003) Developmental gene regulation during tomato fruit ripening and in-vitro sepal morphogenesis. BMC Plant Biol 3:4CrossRefGoogle Scholar
  4. Bartley GE, Ishida BK (2007) Ethylene-sensitive and insensitive regulation of transcription factor expression during in vitro tomato sepal ripening. J Exp Bot 58:2043–2051CrossRefGoogle Scholar
  5. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180CrossRefGoogle Scholar
  6. Bowman JL (2000) The YABBY gene family and abaxial cell fate. Curr Opin Plant Biol 3:17–22CrossRefGoogle Scholar
  7. Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396Google Scholar
  8. Chen C, Xia R, Chen H, He Y (2018) TBtools, a toolkit for biologists integrating various HTS-data handling tools with a user-friendly interface. bioRxiv.  https://doi.org/10.1101/289660 Google Scholar
  9. Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25:1541–1554CrossRefGoogle Scholar
  10. Cheng F, Wu J, Liang J, Wang X (2014) Genome triplication drove the diversification of brassica plants. Hortic Res 1:14024CrossRefGoogle Scholar
  11. Dai M, Zhao Y, Ma Q, Hu Y, Hedden P, Zhang Q, Zhou D-X (2007a) The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiol 144:121–133CrossRefGoogle Scholar
  12. Dai MQ, Hu YF, Zhao Y, Liu HF, Zhou DX (2007b) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144:380–390CrossRefGoogle Scholar
  13. Emery JF et al (2003) Radial patterning of Arabidopsis shoots by class IIIHD-ZIP and KANADI genes. Curr Biol 13:1768–1774CrossRefGoogle Scholar
  14. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260CrossRefGoogle Scholar
  15. Feng C, Jian W, Lu F, Xiaowu W (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198Google Scholar
  16. Finet C, Floyd SK, Conway SJ, Zhong B, Scutt CP, Bowman JL (2016) Evolution of the YABBY gene family in seed plants. Evol Dev 18:116–126CrossRefGoogle Scholar
  17. Franks RG (2010) The molecular organography of plants. Quentin C.B. Cronk integrative and comparative. Biology 50:144–145Google Scholar
  18. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607CrossRefGoogle Scholar
  19. Golz JF, Roccaro M, Kuzoff R, Hudson A (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661–3670CrossRefGoogle Scholar
  20. Huang ZJ, Van Houten J, Gonzalez G, Xiao H, van der Knaap E (2013) Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Mol Genet Genom 288:111–129CrossRefGoogle Scholar
  21. Jonsell B (1991) Weberling, F. 1989. Morphology of flowers and inflorescences. Nord J Bot 11:496–496CrossRefGoogle Scholar
  22. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709CrossRefGoogle Scholar
  23. Kim M, Pham T, Hamidi A, Mccormick S, Kuzoff RK, Sinha N (2003) Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130:4405CrossRefGoogle Scholar
  24. Liu H-l, Xu Y-Y, Xu Z-H, Chong K (2007) A rice YABBY gene, OsYABBY4, preferentially expresses in developing vascular tissue. Dev Genes Evol 217:629–637CrossRefGoogle Scholar
  25. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481Google Scholar
  26. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713CrossRefGoogle Scholar
  27. Nagaharu U (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452Google Scholar
  28. Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25:223–236CrossRefGoogle Scholar
  29. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910CrossRefGoogle Scholar
  30. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45CrossRefGoogle Scholar
  31. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518CrossRefGoogle Scholar
  32. Sawa S, Watanabe K, Goto K, Kanaya E, Morita EH, Okada K (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains (vol 13, pg 1079, 1999). Gene Dev 13:2337CrossRefGoogle Scholar
  33. Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542CrossRefGoogle Scholar
  34. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128Google Scholar
  35. Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105–3118CrossRefGoogle Scholar
  36. Tanaka W et al (2012) The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 24:80–95CrossRefGoogle Scholar
  37. Tong C et al (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genom 14:689CrossRefGoogle Scholar
  38. Toriba T, Harada K, Takamura A, Nakamura H, Ichikawa H, Suzaki T, Hirano HY (2007) Molecular characterization the YABBY gene family in Oryza sativa and expression analysis of OsYABBY1. Mol Genet Genom 277:457–468CrossRefGoogle Scholar
  39. Villanueva JM, Pohl J, Doetsch PW, Marzilli LG (1999) The mutagenic damaged DNA base, 5,6-dihydrouracil (DHU), incorporated into a 14-mer duplex: NMR evidence that DHU is intrahelical and causes minimal DNA distortion. J Am Chem Soc 121:10652–10653CrossRefGoogle Scholar
  40. Waites R, Hudson A (1995) Phantastica—a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154Google Scholar
  41. Wang X et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039CrossRefGoogle Scholar
  42. Yamada T, Ito M, Kato M (2004) YABBY2-homologue expression in lateral organs of Amborella trichopoda (Amborellaceae). Int J Plant Sci 165:917–924CrossRefGoogle Scholar
  43. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Hualan Hou
    • 1
  • Peng Wu
    • 1
  • Liwei Gao
    • 1
  • Changwei Zhang
    • 1
  • Xilin Hou
    • 1
    Email author
  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement/Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture/Engineering Research Center of Germplasm Enhancement and Utilization of Horticultural Crops, Ministry of EducationNanjing Agricultural UniversityNanjingChina

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