Advertisement

Functional & Integrative Genomics

, Volume 18, Issue 6, pp 685–700 | Cite as

Genome-wide identification, expansion, and evolution analysis of homeobox genes and their expression profiles during root development in carrot

  • Feng Que
  • Guang-Long Wang
  • Tong Li
  • Ya-Hui Wang
  • Zhi-Sheng Xu
  • Ai-Sheng Xiong
Original Article

Abstract

The homeobox gene family, a large family represented by transcription factors, has been implicated in secondary growth, early embryo patterning, and hormone response pathways in plants. However, reports about the information and evolutionary history of the homeobox gene family in carrot are limited. In the present study, a total of 130 homeobox family genes were identified in the carrot genome. Specific codomain and phylogenetic analyses revealed that the genes were classified into 14 subgroups. Whole genome and proximal duplication participated in the homeobox gene family expansion in carrot. Purifying selection also contributed to the evolution of carrot homeobox genes. In Gene Ontology (GO) analysis, most members of the HD-ZIP III and IV subfamilies were found to have a lipid binding (GO:0008289) term. Most HD-ZIP III and IV genes also harbored a steroidogenic acute regulatory protein-related lipid transfer (START) domain. These results suggested that the HD-ZIP III and IV subfamilies might be related to lipid transfer. Transcriptome and quantitative real-time PCR (RT-qPCR) data indicated that members of the WOX and KNOX subfamilies were likely implicated in carrot root development. Our study provided a useful basis for further studies on the complexity and function of the homeobox gene family in carrot.

Keywords

Homeobox genes Expansion Evolution GO annotation Root Daucus carota L. 

Abbreviations

DAS

Days after sowing

DD

Dispersed gene duplication

HD

Homeodomain

HD-ZIP

HD-leucine zipper

LD

Luminidependens

LS-WGDs

Lineage-specific WGDs

PD

Proximal duplication

RT-qPCR

Quantitative real-time PCR

TD

Tandem duplication

TSD

DNA-transposed duplication

WGD

Whole genome duplication

WOX

WUSCHEL-like homeobox

Notes

Acknowledgements

The research was supported by the New Century Excellent Talents in University (NCET-11-0670), Jiangsu Natural Science Foundation (BK20130027), and Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author contributions

Conceived and designed the experiments: ASX FQ. Performed the experiments: FQ GLW ZSX TL YHW. Analyzed the data: FQ. Contributed reagents/materials/analysis tools: ASX. Wrote the paper: FQ. Revised the paper: ASX GLW. All authors read and approved the final manuscript.

Supplementary material

10142_2018_624_MOESM1_ESM.pdf (22 mb)
ESM 1 S1 Figure. Multiple sequence alignment of homedomain sequence of all carrot homeobox genes. (PDF 22517 kb)
10142_2018_624_MOESM2_ESM.pdf (914 kb)
ESM 2 S2 Figure. Phylogenetic tree of KNOX genes from carrot and Arabidopsis. (PDF 914 kb)
10142_2018_624_MOESM3_ESM.xlsx (28 kb)
ESM 3 S1 Table. List of 130 carrot homeobox genes and their related information. (XLSX 28 kb)
10142_2018_624_MOESM4_ESM.xlsx (16 kb)
ESM 4 S2 Table. Pfam domain of the 130 carrot homeobox genes. (XLSX 15 kb)
10142_2018_624_MOESM5_ESM.xlsx (26 kb)
ESM 5 S3 Table. List of homeobox genes from Arabidopsis thaliana, Oryza sativa and carrot. (XLSX 25 kb)
10142_2018_624_MOESM6_ESM.xlsx (27 kb)
ESM 6 S4 Table. Ka/Ks values of gene pairs from different duplication modes. (XLSX 27 kb)
10142_2018_624_MOESM7_ESM.xlsx (14 kb)
ESM 7 S5 Table. List of Gene Ontology (GO) ID of carrot homeobox genes. (XLSX 14 kb)

References

  1. Bhattacharjee A, Ghangal R, Garg R, Jain M (2015) Genome-wide analysis of homeobox gene family in legumes: identification, gene duplication and expression profiling. PLoS One 10(3):e0119198CrossRefGoogle Scholar
  2. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16(7):1679–1691CrossRefGoogle Scholar
  3. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):10CrossRefGoogle Scholar
  4. Chan RL, Gago GM, Palena CM, Gonzalez DH (1998) Homeoboxes in plant development. Biochim Biophys Acta Gene Struct Expr 1442(1):1–19CrossRefGoogle Scholar
  5. De Smet R, Adams KL, Vandepoele K, Van Montagu MC, Maere S, Van de Peer Y (2013) Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc Natl Acad Sci 110(8):2898–2903CrossRefGoogle Scholar
  6. Desplan C, Theis J, O'Farrell PH (1988) The sequence specificity of homeodomain-DNA interaction. Cell 54(7):1081–1090CrossRefGoogle Scholar
  7. Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8(1):291CrossRefGoogle Scholar
  8. Di Giacomo E, Laffont C, Sciarra F, Iannelli MA, Frugier F, Frugis G (2017) KNAT3/4/5‐like class 2 KNOX transcription factors are involved in Medicago truncatula symbiotic nodule organ development. New Phytol 213(2):822–837CrossRefGoogle Scholar
  9. Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52(1):17–27CrossRefGoogle Scholar
  10. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195CrossRefGoogle Scholar
  11. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J (2013) Pfam: the protein families database. Nucleic Acids Res 42(D1):D222–D230CrossRefGoogle Scholar
  12. Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR (2015) HMMER web server: 2015 update. Nucleic Acids Res 43(W1):W30–W38CrossRefGoogle Scholar
  13. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453CrossRefGoogle Scholar
  14. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24(10):2298–2309CrossRefGoogle Scholar
  15. Gehring WJ, Affolter M, Burglin T (1994) Homeodomain proteins. Annu Rev Biochem 63(1):487–526CrossRefGoogle Scholar
  16. Groover AT, Mansfield SD, DiFazio SP, Dupper G, Fontana JR, Millar R, Wang Y (2006) The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61(6):917–932CrossRefGoogle Scholar
  17. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu S-H (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148(2):993–1003CrossRefGoogle Scholar
  18. Hedman H, Zhu TQ, Arnold SV, Sohlberg JJ (2013) Analysis of the WUSCHEL-RELATED HOMEOBOX gene family in the conifer Picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biol 13(1):89CrossRefGoogle Scholar
  19. Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22(8):2618–2629CrossRefGoogle Scholar
  20. Holland PW (2013) Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol 2(1):31–45CrossRefGoogle Scholar
  21. Iorizzo M, Ellison S, Senalik D, Zeng P, Satapoomin P, Huang J, Bowman M, Iovene M, Sanseverino W, Cavagnaro P (2016) A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet 48(6):657–666CrossRefGoogle Scholar
  22. Jain M, Tyagi AK, Khurana JP (2008) Genome‐wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J 275(11):2845–2861CrossRefGoogle Scholar
  23. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152(3):1346–1356CrossRefGoogle Scholar
  24. Jørgensen JE, Grønlund M, Pallisgaard N, Larsen K, Marcker KA, Ostergaard Jensen E (1999) A new class of plant homeobox genes is expressed in specific regions of determinate symbiotic root nodules. Plant Mol Biol 40(1):65–77CrossRefGoogle Scholar
  25. Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yammguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6(12):1877–1887CrossRefGoogle Scholar
  26. Larson PR (2012) The vascular cambium: development and structure. Springer, BerlinGoogle Scholar
  27. Lehti-Shiu MD, Zou C, Hanada K, Shiu S-H (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150(1):12–26CrossRefGoogle Scholar
  28. Letunic I, Doerks T, Bork P (2011) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40(D1):D302–D305CrossRefGoogle Scholar
  29. Lynch M (2002) Gene duplication and evolution. Science 297(5583):945–947CrossRefGoogle Scholar
  30. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci U S A 102(15):5454–5459CrossRefGoogle Scholar
  31. Michael TP, VanBuren R (2015) Progress, challenges and the future of crop genomes. Curr Opin Plant Biol 24:71–81CrossRefGoogle Scholar
  32. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628CrossRefGoogle Scholar
  33. Mukherjee K, Brocchieri L, Bürglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26(12):2775–2794CrossRefGoogle Scholar
  34. Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171(4):2294–2316PubMedPubMedCentralGoogle Scholar
  35. Paterson AH, Freeling M, Tang H, Wang X (2010) Insights from the comparison of plant genome sequences. Annu Rev Plant Biol 61:349–372CrossRefGoogle Scholar
  36. Qiao X, Li L, Yin H, Liu X, Wang D, Wu J, Wu J, Zhang S (2015) Modes of gene duplication and gene family expansion and evolution in Chinese white pear. In: Plant and Animal Genome XXIII Conference, January: 2015: 10–14Google Scholar
  37. Ragni L, Hardtke CS (2014) Small but thick enough—the Arabidopsis hypocotyl as a model to study secondary growth. Physiol Plant 151(2):164–171CrossRefGoogle Scholar
  38. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319(5859):64–69CrossRefGoogle Scholar
  39. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446(7137):811–814CrossRefGoogle Scholar
  40. Siebers T, Catarino B, Agusti J (2017) Identification and expression analyses of new potential regulators of xylem development and cambium activity in cassava (Manihot esculenta). Planta 245(3):539–548CrossRefGoogle Scholar
  41. Soltis PS, Marchant DB, Van de Peer Y, Soltis DE (2015) Polyploidy and genome evolution in plants. Curr Opin Genet Dev 35:119–125CrossRefGoogle Scholar
  42. Spicer R, Groover A (2010) Evolution of development of vascular cambia and secondary growth. New Phytol 186(3):577–592CrossRefGoogle Scholar
  43. Stolarczyk J, Janick J (2011) Carrot: history and iconography. Chronica Hortic 51:13–18Google Scholar
  44. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23(9):3247–3259CrossRefGoogle Scholar
  45. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefGoogle Scholar
  46. Tian C, Jiang Q, Wang F, Wang G-L, Xu Z-S, Xiong A-S (2015) Selection of suitable reference genes for qPCR normalization under abiotic stresses and hormone stimuli in carrot leaves. PLoS One 10(2):e0117569CrossRefGoogle Scholar
  47. Veraksa A, Del Campo M, McGinnis W (2000) Developmental patterning genes and their conserved functions: from model organisms to humans. Mol Genet Metab 69(2):85–100CrossRefGoogle Scholar
  48. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78CrossRefGoogle Scholar
  49. Wang Y (2013) Locally duplicated ohnologs evolve faster than nonlocally duplicated ohnologs in Arabidopsis and rice. Genome Biol Evol 5(2):362–369CrossRefGoogle Scholar
  50. Wang Y, Wang X, Tang H, Tan X, Ficklin SP, Feltus FA, Paterson AH (2011) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 6(12):e28150CrossRefGoogle Scholar
  51. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee T-H, Jin H, Marler B, Guo H (2012a) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49–e49CrossRefGoogle Scholar
  52. Wang Y, Wang X, Paterson AH (2012b) Genome and gene duplications and gene expression divergence: a view from plants. Ann N Y Acad Sci 1256(1):1–14CrossRefGoogle Scholar
  53. Wang Y, Tan X, Paterson AH (2013) Different patterns of gene structure divergence following gene duplication in Arabidopsis. BMC Genomics 14(1):652CrossRefGoogle Scholar
  54. Wang G-L, Xiong F, Que F, Xu Z-S, Wang F, Xiong A-S (2015a) Morphological characteristics, anatomical structure, and gene expression: novel insights into gibberellin biosynthesis and perception during carrot growth and development. Hortic Res 2:15028CrossRefGoogle Scholar
  55. Wang G-L, Jia X-L, Xu Z-S, Wang F, Xiong A-S (2015b) Sequencing, assembly, annotation, and gene expression: novel insights into the hormonal control of carrot root development revealed by a high-throughput transcriptome. Mol Gen Genomics 290(4):1379–1391CrossRefGoogle Scholar
  56. Wang G-M, Yin H, Qiao X, Tan X, Gu C, Wang B-H, Cheng R, Wang Y-Z, Zhang S-L (2016) F-box genes: genome-wide expansion, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri). Plant Sci 253:164–175CrossRefGoogle Scholar
  57. Wijnheijmer EHM, Brandenburg WA, Borg SJT (1989) Interactions between wild and cultivated carrots (Daucus carota, L.) in the Netherlands. Euphytica 40(1–2):147–154CrossRefGoogle Scholar
  58. Woerlen N, Allam G, Popescu A, Corrigan L, Pautot V, Hepworth SR (2017) Repression of blade-on-petiole genes by knox homeodomain protein brevipedicellus is essential for differentiation of secondary xylem in Arabidopsis root. Planta 245(6):1079–1090CrossRefGoogle Scholar
  59. Xu Z-S, Tan H-W, Wang F, Hou X-L, Xiong A-S (2014) CarrotDB: a genomic and transcriptomic database for carrot. Database 2014:bau096CrossRefGoogle Scholar
  60. Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics, Proteomics Bioinformatics 4(4):259–263CrossRefGoogle Scholar
  61. Zhang X, Zong J, Liu J, Yin J, Zhang D (2010) Genome‐wide analysis of WOX gene family in rice, sorghum, maize, Arabidopsis and poplar. J Integr Plant Biol 52(11):1016–1026CrossRefGoogle Scholar
  62. Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, Dai L (2012) ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun 419(4):779–781CrossRefGoogle Scholar
  63. Zhong YF, Holland PW (2011) HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology. Evol Dev 13(6):567–568CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Feng Que
    • 1
  • Guang-Long Wang
    • 1
  • Tong Li
    • 1
  • Ya-Hui Wang
    • 1
  • Zhi-Sheng Xu
    • 1
  • Ai-Sheng Xiong
    • 1
  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of HorticultureNanjing Agricultural UniversityNanjingChina

Personalised recommendations