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Transcriptome analyses provide insights into development of the Zingiber zerumbet flower, revealing potential genes related to floral organ formation and patterning

  • Tong Zhao
  • Chelsea D. Specht
  • Zhicheng Dong
  • Yushi Ye
  • Huanfang LiuEmail author
  • Jingping Liao
Original paper

Abstract

The flower of Zingiber zerumbet is characterized by a distinctive labellum, a highly modified floral organ believed to be formed by the fusion of several infertile members of the androecial whorl (staminodes). Across the Zingiberaceae, the number of staminodes involved in labellum formation varies from two to four, and these are reflected in the number of lobes that comprise the mature labellum. Research on the flower development in Zingiberaceae has been limited to species with either no labellum lobes or species displaying a bilobed labellum. Zingiber zerumbet is a representative of the genus with a three-lobed labellum, and its flower development remains poorly understood at both morphological and molecular levels. This study aims to give a comprehensive description of its flower development and to identify potential genes related to flower development using morphological and genetic characterization. Our results show that floral organ initiation is sequential with the sepal whorl initiating first, followed by petal and inner androecium together, followed by outer androecium, and finally the initiation of the inferior gynoecium. The three-lobed labellum comprises four androecial members: Two abaxial inner androecial members fuse to form the single central lobe, and two adaxial outer androecial members individually form the two lateral lobes of the labellum. Two developmental stages (floral primordium and organ-differentiated flowers) were selected for transcriptome sequencing. Two-thousand and seventy-five transcription factors were identified. Seven boundary genes and seven organ-specific genes were also discovered. Our study provides fundamental information for further studies on the molecular mechanisms of flower development and evolution across the Zingiberaceae.

Keywords

Flower development Labellum Transcriptome Floral organ fusion Zingiber zerumbet 

Notes

Acknowledgements

This work is supported by the National Natural Science Foundation of China (Grant Nos. 31670336, 31200246, 31271318) and Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences (Grant No. Y821171001). We thank Haoran Ding for his assistance with part of the experiments.

Author contributions

TZ performed the experiments, analyzed the data and wrote the manuscript. HFL designed the research and performed the experiments. CDS and ZCD performed parts of the data analysis and CDS helped write parts of the discussion. YSY and JPL provided assistance with samples collection and offered some photos of Z. zerumbet. All authors contributed to the manuscript revision.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10725_2020_575_MOESM1_ESM.xlsx (33 kb)
Supplementary file1 (XLSX 33 kb)
10725_2020_575_MOESM2_ESM.pdf (844 kb)
Supplementary file2 (PDF 843 kb)

References

  1. Aida M, Ishida T, Fukaki H et al (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857PubMedPubMedCentralGoogle Scholar
  2. Almeida AMR, Brown A, Specht CD (2013) Tracking the development of the petaloid fertile stamen in Canna indica: insights into the origin of androecial petaloidy in the Zingiberales. AoB Plants 5:1–7CrossRefGoogle Scholar
  3. Almeida AMR, Yockteng R, Schnable J et al (2014) Co-option of the polarity gene network shapes filament morphology in angiosperms. Sci Rep 4:6194PubMedPubMedCentralCrossRefGoogle Scholar
  4. Almeida AMR, Yockteng R, Otoni WC, Specht CD (2015a) Positive selection on the K domain of the AGAMOUS protein in the Zingiberales suggests a mechanism for the evolution of androecial morphology. Evodevo 6:1–15CrossRefGoogle Scholar
  5. Almeida AMR, Yockteng R, Specht CD (2015b) Evolution of petaloidy in the Zingiberales: an assessment of the relationship between ultrastructure and gene expression patterns. Dev Dyn 244:1121–1132CrossRefGoogle Scholar
  6. Almeida AMR, Pineyro-Nelson A, Yockteng R et al (2018) Comparative analysis of whole flower transcriptomes in the Zingiberales. PeerJ 6:e5490PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bartlett ME, Specht CD (2010) Evidence for the involvement of GLOBOSA-like gene duplications and expression divergence in the evolution of floral morphology in the Zingiberales. New Phytol 187:521–541PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bell EM, Lin WC, Husbands AY et al (2012) Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci USA 109:21146–21151PubMedCrossRefPubMedCentralGoogle Scholar
  9. Belles-Boix E, Hamant O, Witiak SM et al (2006) KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell 18:1900–1907PubMedPubMedCentralCrossRefGoogle Scholar
  10. Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bowman JL, Smyth DR, Meyerowitz EM, Meyerowitzt EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedPubMedCentralGoogle Scholar
  12. Brewer PB, Howles PA, Dorian K et al (2004) PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower. Development 131:4035–4045PubMedCrossRefPubMedCentralGoogle Scholar
  13. Causier B, Schwarz-Sommer Z, Davies B (2010) Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 21:73–79PubMedCrossRefGoogle Scholar
  14. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  15. Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle Scholar
  16. Costerus JC (1915) Das Labellum und das Diagram der Zingiberaceen. Ann Jardin Botanique Buitenzorg II 14:95–108Google Scholar
  17. D’Hont A, Denoeud F, Aury JM et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217PubMedCrossRefGoogle Scholar
  18. Ditta G, Pinyopich A, Robles P et al (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940PubMedCrossRefGoogle Scholar
  19. Eichler AW (1884) Uber den bluthenbau der Zingiberaceen. Sitzungsber der Königlich Preuss. Akad Wiss 26:585–600Google Scholar
  20. Endress PK (2011) Evolutionary diversification of the flowers in angiosperms. Am J Bot 98(3):370–396PubMedCrossRefPubMedCentralGoogle Scholar
  21. Fu Q, Liu H, Almeida AMR et al (2014) Molecular basis of floral petaloidy: insights from androecia of Canna indica. AoB Plants 6:490–552CrossRefGoogle Scholar
  22. Grabherr MG, Haas BJ, Yassour M et al (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644–652PubMedPubMedCentralCrossRefGoogle Scholar
  23. He J, Jiao Y (2014) Next-generation sequencing applied to flower development: RNA-seq. In: Riechmann JL, Wellmer F (eds) Flower development: methods and protocols, vol 1110. Springer, New York, pp 401–411CrossRefGoogle Scholar
  24. Huang JZ, Lin CP, Cheng TC et al (2015) A de novo floral transcriptome reveals clues into Phalaenopsis orchid flower development. PLoS ONE 10:1–20Google Scholar
  25. Kirchoff BK (1983) Floral organogenesis in five genera of the Marantaceae and in Canna (Cannaceae). Am J Bot 70:508–523CrossRefGoogle Scholar
  26. Kirchoff BK (1988a) Floral ontogeny and evolution in the ginger group of the Zingiberales. In: Leins P, Tucker SC, Endress PK (eds) Aspects of floral development. Cramer, Berlin, pp 45–56Google Scholar
  27. Kirchoff BK (1988b) Inflorescence and flower development in Costus scaber (Costaceae). Can J Bot 62:339–345CrossRefGoogle Scholar
  28. Kirchoff BK (1991) Homeosis in the flowers of the Zingiberales. Am J Bot 78:833–837CrossRefGoogle Scholar
  29. Kirchoff BK (1997) Inflorescence and flower development in the Hedychieae (Zingiberaceae): Hedychium. Can J Bot 75:581–594CrossRefGoogle Scholar
  30. Kirchoff BK (1998) Inflorescence and flower development in the Hedychieae (Zingiberaceae): Scaphochlamys kunstleri (Baker) Holttum. Int J Plant Sci 159(2):261–274CrossRefGoogle Scholar
  31. Kirchoff BK, Lagomarsino LP, Newman WH et al (2009) Early floral development of Heliconia latispatha (Heliconiaceae), a key taxon for understanding the evolution of flower development in the Zingiberales. Am J Bot 96:580–593PubMedCrossRefPubMedCentralGoogle Scholar
  32. Krizek BA, Lewis MW, Fletcher JC (2006) RABBIT EARS is a second-whorl repressor of AGAMOUS that maintains spatial boundaries in Arabidopsis flowers. Plant J 45:369–383PubMedCrossRefPubMedCentralGoogle Scholar
  33. Lampugnani ER, Kilinc A, Smyth DR (2012) PETAL LOSS is a boundary gene that inhibits growth between developing sepals in Arabidopsis thaliana. Plant J 71:724–735PubMedCrossRefPubMedCentralGoogle Scholar
  34. Lestiboudois T (1829) Notice sur le genre Hedychium de la famille des Musacees (Balisiers et Bananiers). Annu Sci Natl Premium Service 17:113–139Google Scholar
  35. Li W, Zhang L, Ding Z et al (2017) De novo sequencing and comparative transcriptome analysis of the male and hermaphroditic flowers provide insights into the regulation of flower formation in andromonoecious Taihangia rupestris. BMC Plant Biol 17:1–19PubMedPubMedCentralCrossRefGoogle Scholar
  36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆Ct method. Methods 25:402–408PubMedPubMedCentralCrossRefGoogle Scholar
  37. Mahadevan C, Jaleel A, Deb L et al (2015) Development of an efficient virus induced gene silencing strategy in the non-model wild ginger-Zingiber zerumbet and investigation of associated proteome changes. PLoS ONE 10:1–17CrossRefGoogle Scholar
  38. Morioka K, Yockteng R, Almeida AMR et al (2015) Loss of YABBY2-Like gene expression may underlie the evolution of the laminar style in Canna and contribute to floral morphological diversity in the Zingiberales. Front Plant Sci 6:1106PubMedPubMedCentralCrossRefGoogle Scholar
  39. Pelaz S, Ditta GS, Baumann E et al (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203PubMedCrossRefGoogle Scholar
  40. Piñeyro-Nelson A, Almeida AMR, Sass C et al (2017) Change of fate and staminodial laminarity as potential agents of floral diversification in the Zingiberales. J Exp Zool B 328:41–54CrossRefGoogle Scholar
  41. Renner T, Bragg J, Driscoll HE et al (2009) Viral induced gene silencing as a tool for investigating floral developmental genetics in the Zingiberales. Mol Plant 3:1–11Google Scholar
  42. Robinson MD, McCarthy DJ, Smyth GK (2009) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140PubMedPubMedCentralCrossRefGoogle Scholar
  43. Sakai H, Medrano LJ, Meyerowitz EM (1995) Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378:199–203PubMedCrossRefPubMedCentralGoogle Scholar
  44. Sass C, Iles WJD, Barrett CF et al (2016) Revisiting the Zingiberales: using multiplexed exon capture to resolve ancient and recent phylogenetic splits in a charismatic plant lineage. PeerJ 4:e1584PubMedPubMedCentralCrossRefGoogle Scholar
  45. Schachner J (1924) Beitrage zur Kenntnis der Bluten und Samenentwicklung der Scitamineen. Flora 117:16–40Google Scholar
  46. Schumann K (1904) Zingiberaceae. Pflanzenreich 20(4):46Google Scholar
  47. Shuai B, Reynaga-Pena CG, Springer PS (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol 129:747–761PubMedPubMedCentralCrossRefGoogle Scholar
  48. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedPubMedCentralGoogle Scholar
  49. Song JJ, Ma W, Tang YJ et al (2010) Isolation and characterization of three MADS-box Genes from Alpinia hainanensis (Zingiberaceae). Plant Mol Biol Report 28:264–276CrossRefGoogle Scholar
  50. Specht CD, Almeida AMR (2017) A process-based approach to the study of flower morphological variation. In: Nuño de la Rosa L, Müller G (eds) Evolutionary developmental biology. Springer, Cham, pp 1–15Google Scholar
  51. Specht CD, Howarth DG (2015) Adaptation in flower form: a comparative evodevo approach. New Phytol 206:74–90PubMedCrossRefPubMedCentralGoogle Scholar
  52. Specht CD, Yockteng R, Almeida AMR et al (2012) Homoplasy, pollination, and emerging complexity during the evolution of floral development in the tropical gingers (Zingiberales). Bot Rev 78:440–462CrossRefGoogle Scholar
  53. Takeda S, Hanano K, Kariya A et al (2011) CUP-SHAPED COTYLEDON1 transcription factor activates the expression of LSH4 and LSH3, two members of the ALOG gene family, in shoot organ boundary cells. Plant J 66:1066–1077PubMedCrossRefPubMedCentralGoogle Scholar
  54. Theiβen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85CrossRefGoogle Scholar
  55. Tian X, Yu Q, Liu H et al (2016) Temporal-spatial transcriptome analyses provide insights into the development of petaloid androecium in Canna indica. Front Plant Sci 7:1–11Google Scholar
  56. Wake DB, Wake MH, Specht CD (2011) Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331:1032–1035PubMedCrossRefPubMedCentralGoogle Scholar
  57. Wang Q, Hasson A, Rossmann S et al (2016) Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytol 209:485–498PubMedCrossRefGoogle Scholar
  58. Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209PubMedCrossRefGoogle Scholar
  59. Yob NJ, Jofrry SM, Affandi MM et al (2011) Zingiber zerumbet (L.) Smith: a review of its ethnomedicinal, chemical, and pharmacological uses. Evidence-based Complement Altern Med 2011:1–12CrossRefGoogle Scholar
  60. Yockteng R, Almeida AMR, Morioka K et al (2013) Molecular evolution and patterns of duplication in the SEP/AGL6-like lineage of the Zingiberales: a proposed mechanism for floral diversification. Mol Biol Evol 30:2401–2422PubMedCrossRefPubMedCentralGoogle Scholar
  61. Yockteng R, Almeida AMR, Piñeyro-Nelson A, Specht CD (2014) Adaptation of floral form: an evo-devo approach to study adaptive evolution in floral morphology. In: Laitinen R (ed) Molecular mechanisms in plant adaptation. Wiley, New York, pp 171–192Google Scholar
  62. Zhang J, Wu K, Zeng S et al (2013) Transcriptome analysis of Cymbidium sinense and its application to the identification of genes associated with floral development. BMC Genomics 14:279PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  • Tong Zhao
    • 1
    • 2
  • Chelsea D. Specht
    • 3
  • Zhicheng Dong
    • 4
  • Yushi Ye
    • 5
  • Huanfang Liu
    • 1
    Email author
  • Jingping Liao
    • 1
  1. 1.Key Laboratory of Plant Resources Conservation and Sustainable Utilization, Guangdong Provincial Key Laboratory of Digital Botanical Garden, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.College of Life SciencesUniversity of Chinese Academy of SciencesBeijingChina
  3. 3.School of Integrative Plant Sciences, Section of Plant Biology and the L.H. Bailey HortoriumCornell UniversityIthacaUSA
  4. 4.School of Life SciencesGuangzhou UniversityGuangzhouChina
  5. 5.Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, South China Botanical GardenChinese Academy of SciencesGuangzhouChina

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