Abstract
Gaillardia plants have been widely cultivated in China and have become an important component of garden landscaping. Different from the common ligulate ray floret, the cornflower-like (funnel-shaped) ray floret is a special phenotype variation in Gaillardia species. Previous studies revealed that CYC-like genes could shape the floret phenotype in Compositae. To reveal the molecular mechanism of the cornflower-like phenotype, we checked the capitulum transcriptomes of several cultivars of Gaillardia that possess different ray florets. As a result, we identified 11 CYC-like genes, of which five included complete coding region sequences. Phylogenetic analysis revealed that all five genes were CYC2-like genes. Relative expression analysis of RNA-resequencing reads, qRT-PCR comparison, and gene-silencing treatment all showed that the CYC2c gene is the main genetic mechanism responsible for the shaping of the cornflower-like ray floret phenotype in Gaillardia cultivars. This study expounded our understanding of flower morphology evolution and provides useful insights for improving Compositae breeding.
This is a preview of subscription content, access via your institution.





Data availability
The authors declare that all data supporting the findings of this study are provided in full in the results section of this paper.
References
Bello MA, Cubas P, Alvarez I, Sanjuanbenito G, Fuertes-Aguilar J (2017) Evolution and expression patterns of CYC/TB1 genes in Anacyclus: phylogenetic insights for floral symmetry genes in Asteraceae. Front Plant Sci 8:589. https://doi.org/10.3389/fpls.2017.00589
Broholm SK, Tahtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa P (2008) A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Natl Acad Sci USA 105:9117–9122. https://doi.org/10.1073/pnas.0801359105
Chapman MA, Leebens-Mack JH, Burke JM (2008) Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Mol Biol Evol 25:1260–1273. https://doi.org/10.1093/molbev/msn001
Chapman MA, Tang S, Draeger D, Nambeesan S, Shaffer H, Barb JG, Knapp SJ, Burke JM (2012) Genetic analysis of floral symmetry in Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae. PLoS Genet 8:e1002628. https://doi.org/10.1371/journal.pgen.1002628
Chen J, Shen CZ, Guo YP, Rao GY (2018) Patterning the asteraceae capitulum: duplications and differential expression of the flower symmetry CYC2-like genes. Front Plant Sci 9:551. https://doi.org/10.3389/fpls.2018.00551
Damerval C, Le Guilloux M, Jager M, Charon C (2007) Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. Plant Physiol 143:759–772. https://doi.org/10.1104/pp.106.090324
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488. https://doi.org/10.1038/386485a0
Fambrini M, Bernardi R, Pugliesi C (2020) Ray flower initiation in the Helianthus radula inflorescence is influenced by a functional allele of the HrCYC2c gene. Genesis 58:e23401. https://doi.org/10.1002/dvg.23401
Gouy M, Tannier E, Comte N, Parsons DP (2021) Seaview version 5: a multiplatform software for multiple sequence alignment, molecular phylogenetic analyses, and tree reconciliation. Methods Mol Biol 2231:241–260. https://doi.org/10.1007/978-1-0716-1036-7_15
Hileman LC (2014) Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philos Trans R Soc Lond B Biol Sci 369:20130348. https://doi.org/10.1098/rstb.2013.0348
Howarth DG, Donoghue MJ (2006) Phylogenetic analysis of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA 103:9101–9106. https://doi.org/10.1073/pnas.0602827103
Huang D, Li X, Sun M, Zhang T, Pan H, Cheng T, Wang J, Zhang Q (2016) Identification and characterization of CYC-like genes in regulation of ray floret development in Chrysanthemum morifolium. Front Plant Sci 7:1633. https://doi.org/10.3389/fpls.2016.01633
Karsai A, Muller S, Platz S, Hauser MT (2002) Evaluation of a homemade SYBR green I reaction mixture for real-time PCR quantification of gene expression. Biotechniques 32(790–792):794–796. https://doi.org/10.2144/02324st05
Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619. https://doi.org/10.1105/tpc.9.9.1607
Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799. https://doi.org/10.1038/383794a0
Martin-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39. https://doi.org/10.1016/j.tplants.2009.11.003
Mizzotti C, Fambrini M, Caporali E, Masiero S, Pugliesi C (2015) A CYCLOIDEA-like gene mutation in sunflower determines an unusual floret type able to produce filled achenes at the periphery of the pseudanthium. Botany 93:171–181. https://doi.org/10.1139/cjb-2014-0210
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Spencer V, Kim M (2018) Re”CYC”ing molecular regulators in the evolution and development of flower symmetry. Semin Cell Dev Biol 79:16–26. https://doi.org/10.1016/j.semcdb.2017.08.052
Tahtiharju S, Rijpkema AS, Vetterli A, Albert VA, Teeri TH, Elomaa P (2012) Evolution and diversification of the CYC/TB1 gene family in Asteraceae-a comparative study in Gerbera (Mutisieae) and sunflower (Heliantheae). Mol Biol Evol 29:1155–1166. https://doi.org/10.1093/molbev/msr283
Tanaka Y, Yamamura T, Oshima Y, Mitsuda N, Koyama T, Ohme-Takagi M, Terakawa T (2011) Creating ruffled flower petals in Cyclamen persicum by expression of the chimeric cyclamen TCP repressor. Plant Biotechnol 28:141–147. https://doi.org/10.5511/plantbiotechnology.10.1227a
Xu S, Luo Y, Cai Z, Cao X, Hu X, Yang J, Luo D (2013) Functional diversity of CYCLOIDEA-like TCP genes in the control of zygomorphic flower development in Lotus japonicus. J Integr Plant Biol 55:221–231. https://doi.org/10.1111/j.1744-7909.2012.01169.x
Zhang JS, Zhao J, Zhang S, He C (2014) Efficient gene silencing mediated by tobacco rattle virus in an emerging model plant physalis. PLoS ONE 9:e85534. https://doi.org/10.1371/journal.pone.0085534
Zheng L, Zhou XJ, Ma Y, Guo MX (2019) Genome-wide identification and characterization of TCP family genes associated with flower and fruit development in Fragaria Vesca. Pak J Bot 51:513–519. https://doi.org/10.30848/Pjb2019-2(16)
Acknowledgements
We would like to thank Miss Xin Xu, Hongyan Liu, and Shuting Yue for assistance with seed collection and transcriptome sampling. We thank Editage (http://www.editage.cn) for English language editing.
Funding
This work was supported by the National Natural Science Foundation of China (32070246).
Author information
Authors and Affiliations
Contributions
YB designed the study. PS, YB, YJZ, NH, and XRW performed the experiments. YJZ and ZYW cultivated the plant materials. PS and YB analyzed the data and wrote the manuscript. All authors read and approved of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sun, P., Bao, Y., Zhu, Y. et al. Possible role of the CYC2c gene in the cornflower-like ray floret phenotype of Gaillardia cultivars. J Plant Res 135, 465–472 (2022). https://doi.org/10.1007/s10265-022-01379-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-022-01379-8
Keywords
- Blanket flower
- CYCLOIDEA gene
- Funnel-shaped florets