Abstract
Key message
The overexpression of HaCYC2c and its regulation on HaNDUA2 through transcriptional recognition are important for regulating the heteromorphous development and functional differentiation of ray and disc florets in sunflower.
Abstract
Flower symmetry is closely related to pollinator recruitment and individual fecundity for higher plants and is the main feature used to identify flower type in angiosperms. In sunflower, HaCYC2c regulates floral organ development and floral symmetry, but the specific detail remains unclear. In this study, sunflower long petal mutant (lpm) with HaCYC2c insertion mutation was used to investigate the regulating role of HaCYC2c in the morphogenesis of florets and the transformation of floral symmetry through phenotype, transcriptome, qRT-PCR, and possible protein-gene interactions analyses. Results showed that HaCYC2c was overexpressed after an insertion into the promoter region. This gene could recognize the cis-acting element GGTCCC in the promoter region of HaNDUA2 that might regulate HaNDUA2 and affect other related genes. As a consequence, the abnormal elongation of disc petals and the degradation of male reproductive system occurred at the early development of floral organ in sunflower. Furthermore, this insertion mutation resulted in floral symmetry transformation, from actinomorphy to zygomorphy, thereby making the tubular disc florets transformed into ray-like disc florets in sunflower lpm. The findings suggested that the overexpression of HaCYC2c and its control of HaNDUA2 through transcriptional recognition might be an important regulating node of the heteromorphous development and functional differentiation for ray and disc florets in sunflower. This node contributes to the understanding of the balance between pollinator recruitment capacity of ray florets and fertility of disc florets for the optimization of reproductive efficiency and enhancement of species competitiveness in sunflower.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The RNA-seq data and materials can be available for distribution upon request by contacting the corresponding author, Jun Yang (yangjun@cwnu.edu.cn) and Jian Zou (zoujian@cwnu.edu.cn). Other data supporting our findings can be found in the Supplementary Supporting Information.
References
Alvarez-Buylla ER, Benítez M, Corvera-Poiré A, Cador ÁC, de Folter S, de Buen AG, Garay-Arroyo A, García-Ponce B, Jaimes-Miranda F, Pérez-Ruiz RV (2010) Flower development. Arabidopsis Book 8:0127. https://doi.org/10.1199/2Ftab.0127
Andersson S (2008) Pollinator and nonpollinator selection on ray morphology in Leucanthemum vulgare (oxeye daisy, Asteraceae). Am J Bot 95:1072–1078. https://doi.org/10.3732/ajb.0800087
Armbruster WS, Muchhala N (2020) Floral reorientation: the restoration of pollination accuracy after accidents. New Phytol 227:232–243. https://doi.org/10.1111/nph.16482
Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443–448. https://doi.org/10.1038/nature11871
Berger BA, Ambrose BA, Tong J, Howarth DG (2021) Flower development in Fedia graciliflora and Valerianella locusta (Valerianaceae). Flora 275:151754. https://doi.org/10.1016/j.flora.2020.151754
Bukhari G, Zhang J, Stevens PF, Zhang W (2017) Evolution of the process underlying floral zygomorphy development in pentapetalous angiosperms. Am J Bot 104:1846–1856. https://doi.org/10.3732/ajb.1700229
Busch A, Zachgo S (2007) Control of corolla monosymmetry in the Brassicaceae Iberis amara. Proc Natl Acad Sci 104:16714–16719. https://doi.org/10.1073/pnas.0705338104
Busch A, Zachgo S (2009) Flower symmetry evolution: towards understanding the abominable mystery of angiosperm radiation. BioEssays 31:1181–1190. https://doi.org/10.1002/bies.200900081
Carlson SE, Howarth DG, Donoghue MJ (2011) Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. BMC Evol Biol 11:325. https://doi.org/10.1186/1471-2148-11-325
Chanderbali AS, Berger BA, Howarth DG, Soltis PS, Soltis DE (2016) Evolving ideas on the origin and evolution of flowers: new perspectives in the genomic era. Genetics 202:1255–1265. https://doi.org/10.1534/genetics.115.182964
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
Chi X, Dong F, Yang Q, Chen M, Chen N, Pan L, Wang T, Wang M, Yang Z, He Y (2014) Expression and characterization of Lysophosphatidyl acyltransferase genes from peanut (Arachis hypogaea L.). Res Crops 15:141–153. https://doi.org/10.5958/j.2348-7542.15.1.020
Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci 102:5068–5073. https://doi.org/10.1073/pnas.0501340102
Deng X, Gu L, Liu C, Lu T, Lu F, Lu Z, Cui P, Pei Y, Wang B, Hu S (2010) Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing. Proc Natl Acad Sci 107:19114–19119. https://doi.org/10.1073/pnas.1009669107
Endress PK (1999) Symmetry in flowers: diversity and evolution. Int J Plant Sci 160:S3–S23. https://doi.org/10.1086/314211
Endress PK (2012) The immense diversity of floral monosymmetry and asymmetry across angiosperms. Bot Rev 78:345–397. https://doi.org/10.1007/s12229-012-9106-3
Fambrini M, Pugliesi C (2017) CYCLOIDEA 2 clade genes: key players in the control of floral symmetry, inflorescence architecture, and reproductive organ development. Plant Mol Biol Rep 35:20–36. https://doi.org/10.1007/s11105-016-1005-z
Fambrini M, Salvini M, Pugliesi C (2011) A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus. Genetica 139:1521–1529. https://doi.org/10.1007/s10709-012-9652-y
Feng X, Zhao Z, Tian Z, Xu S, Luo Y, Cai Z, Wang Y, Yang J, Wang Z, Weng L (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci 103:4970–4975. https://doi.org/10.1073/pnas.0600681103
Gao Y, Liu Y, Liang Y, Lu J, Jiang C, Fei Z, Jiang CZ, Ma C, Gao J (2019) Rosa hybrida RhERF1 and RhERF4 mediate ethylene-and auxin-regulated petal abscission by influencing pectin degradation. Plant J 99:1159–1171. https://doi.org/10.1111/tpj.14412
Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JA, Coen E, Doonan JH (2000) The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122:1137–1148. https://doi.org/10.1104/pp.122.4.1137
Gorgoni B, Gray NK (2004) The roles of cytoplasmic poly (A)-binding proteins in regulating gene expression: a developmental perspective. Brief Funct Genom 3:125–141. https://doi.org/10.1093/bfgp/3.2.125
Hileman LC (2014) Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances. Philos Trans R Soc B 369:20130348. https://doi.org/10.1098/rstb.2013.0348
Huang T, Irish VF (2015) Temporal control of plant organ growth by TCP transcription factors. Curr Biol 25:1765–1770. https://doi.org/10.1016/j.cub.2015.05.024
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
Jabbour F, Ronse De Craene LP, Nadot S, Damerval C (2009) Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae). Ann Bot 104:809–822. https://doi.org/10.1093/aob/mcp162
Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucl Acids Res 45:D1040–D1045. https://doi.org/10.1093/nar/gkw982
Khaskheli AJ, Ahmed W, Ma C, Zhang S, Liu Y, Li Y, Zhou X, Gao J (2018) RhERF113 functions in ethylene-induced petal senescence by modulating cytokinin content in rose. Plant Cell Physiol 59:2442–2451. https://doi.org/10.1093/pcp/pcy162
Kim HU, Huang AH (2004) Plastid lysophosphatidyl acyltransferase is essential for embryo development in Arabidopsis. Plant Physiol 134:1206–1216. https://doi.org/10.1104/pp.103.035832
Kim HU, Li Y, Huang AH (2005) Ubiquitous and endoplasmic reticulum–located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 17:1073–1089. https://doi.org/10.1105/tpc.104.030403
Kühn U, Wahle E (2004) Structure and function of poly (A) binding proteins. Biochim Et Biophys Acta (BBA) 1678:67–84. https://doi.org/10.1016/j.bbaexp.2004.03.008
Lee K, Han JH, Park YI, Colas des Francs-Small C, Small I, Kang H (2017) The mitochondrial pentatricopeptide repeat protein PPR19 is involved in the stabilization of NADH dehydrogenase 1 transcripts and is crucial for mitochondrial function and Arabidopsis thaliana development. New Phytol 215:202–216. https://doi.org/10.1111/nph.14528
Lian X, Zhang H, Zeng J, Wang Y, Bai X, Liu Q, Zuo T, Zhang Y, Converse R, Zhu L (2020) C2H2-like zinc finger protein 1 causes pollen and pistil malformation through the auxin pathway. Plant Growth Regul 90:505–518. https://doi.org/10.1007/s10725-019-00568-1
Liu J, Wu J, Yang X, Wang YZ (2021) Regulatory pathways of CYC-like genes in patterning floral zygomorphy exemplified in Chirita pumila. J Syst Evol 59:567–580. https://doi.org/10.1111/jse.12574
Lucibelli F, Valoroso MC, Aceto S (2020) Radial or bilateral? The molecular basis of floral symmetry. Genes 11:395. https://doi.org/10.3390/genes11040395
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
Manassero NGU, Viola IL, Welchen E, Gonzalez DH (2013) TCP transcription factors: architectures of plant form. Biomol Concepts 4:111–127. https://doi.org/10.1515/bmc-2012-0051
Mangus DA, Evans MC, Jacobson A (2003) Poly (A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4:223. https://doi.org/10.1186/gb-2003-4-7-223
Mitchell CH, Diggle PK (2005) The evolution of unisexual flowers: morphological and functional convergence results from diverse developmental transitions. Am J Bot 92:1068–1076. https://doi.org/10.3732/ajb.92.7.1068
Naghiloo S (2020) Patterns of symmetry expression in Angiosperms: developmental and evolutionary lability. Front Ecol Evol 8:104. https://doi.org/10.3389/fevo.2020.00104
Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195. https://doi.org/10.1038/35056041
Podgórska A, Burian M, Gieczewska K, Ostaszewska-Bugajska M, Zebrowski J, Solecka D, Szal B (2017) Altered cell wall plasticity can restrict plant growth under ammonium nutrition. Front Plant Sci 8:1344. https://doi.org/10.3389/fpls.2017.01344
Preston JC, Hileman LC (2009) Developmental genetics of floral symmetry evolution. Trends Plant Sci 14:147–154. https://doi.org/10.1016/j.tplants.2008.12.005
Preston JC, Martinez CC, Hileman LC (2011) Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome. Proc Natl Acad Sci 108:2343–2348. https://doi.org/10.1073/pnas.1011361108
Primm TP, Walker KW, Gilbert HF (1996) Facilitated protein aggregation: effects of calcium on the chaperone and anti-chaperone activity of protein disulfide-isomerase. J Biol Chem 271:33664–33669. https://doi.org/10.1074/jbc.271.52.33664
Raimundo J, Sobral R, Bailey P, Azevedo H, Galego L, Almeida J, Coen E, Costa MMR (2013) A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in Antirrhinum flower asymmetry. Plant J 75:527–538. https://doi.org/10.1111/tpj.12225
Raimundo J, Sobral R, Laranjeira S, Costa MMR (2018) Successive domain rearrangements underlie the evolution of a regulatory module controlled by a small interfering peptide. Mol Biol Evol 35:2873–2885. https://doi.org/10.1093/molbev/msy178
Rudall PJ, Bateman RM (2004) Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytol 162:25–44. https://doi.org/10.1111/j.1469-8137.2004.01032.x
Sablowski R (2010) Genes and functions controlled by floral organ identity genes. Semin Cell Dev Biol 21:94–99. https://doi.org/10.1016/j.semcdb.2009.08.008
Sanchez SE, Petrillo E, Beckwith EJ, Zhang X, Rugnone ML, Hernando CE, Cuevas JC, Herz MAG, Depetris-Chauvin A, Simpson CG (2010) A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468:112–116. https://doi.org/10.1038/nature09470
Schininà ME, Maritano S, Barra D, Mondovì B, Marchesini A (1996) Mavicyanin, a stellacyanin-like protein from zucchini peelings: primary structure and comparison with other cupredoxins. Biochim Et Biophys Acta (BBA) 1297:28–32. https://doi.org/10.1016/0167-4838(96)00079-9
Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier P, Dauzat M, Heurtevin L, Guyon V, Takenaka M (2012) PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24:676–691. https://doi.org/10.1105/tpc.111.091074
Tähtiharju 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
Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K-U, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149. https://doi.org/10.1007/978-94-011-4221-2_6
Tucker SC (1999) Evolutionary lability of symmetry in early floral development. Int J Plant Sci 160:S25–S39. https://doi.org/10.1086/314212
van Es SW, Silveira SR, Rocha DI, Bimbo A, Martinelli AP, Dornelas MC, Angenent GC, Immink RG (2018) Novel functions of the Arabidopsis transcription factor TCP 5 in petal development and ethylene biosynthesis. Plant J 94:867–879. https://doi.org/10.1111/tpj.13904
Vincent CA, Coen ES (2004) A temporal and morphological framework for flower development in Antirrhinum majus. Can J Bot 82:681–690. https://doi.org/10.1139/b04-042
Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Et Biophys Acta (BBA) 1699:35–44. https://doi.org/10.1016/j.bbapap.2004.02.017
Yang X, Pang HB, Liu BL, Qiu ZJ, Gao Q, Wei L, Dong Y, Wang YZ (2012) Evolution of double positive autoregulatory feedback loops in CYCLOIDEA2 clade genes is associated with the origin of floral zygomorphy. Plant Cell 24:1834–1847. https://doi.org/10.1105/tpc.112.099457
Yoshizaki M, Furumoto T, Hata S, Shinozaki M, Izui K (2000) Characterization of a novel gene encoding a phytocyanin-related protein in morning glory (Pharbitis nil). Biochem Biophys Res Commun 268:466–470. https://doi.org/10.1006/bbrc.2000.2130
Zhang W, Kramer EM, Davis CC (2010) Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proc Natl Acad Sci 107:6388–6393. https://doi.org/10.1073/pnas.0910155107
Zhao Y, Pfannebecker K, Dommes AB, Hidalgo O, Becker A, Elomaa P (2018) Evolutionary diversification of CYC/TB1-like TCP homologs and their recruitment for the control of branching and floral morphology in Papaveraceae (basal eudicots). New Phytol 220:317–331. https://doi.org/10.1111/nph.15289
Zhong C, Xu H, Ye S, Wang S, Li L, Zhang S, Wang X (2015) Gibberellic acid-stimulated Arabidopsis6 serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in Arabidopsis. Plant Physiol 169:2288–2303. https://doi.org/10.1104/pp.15.00858
Funding
This work is financially supported by National Natural Science Fund of China (31171587), Talent Fund of China West Normal University (17YC354), 2018 Doctoral Scientific Research Startup Found of China West Normal University (18Q039), National General Training Fund of West China Normal University (19B035), Innovation Team Project of China West Normal University (Grant No. CXTD2018-6), Key Training Project of Sichuan Provincial Department of Education (14CZ0015).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Leandro Peña.
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
He, Z., Zeng, W., Chen, W. et al. HaCYC2c regulating the heteromorphous development and functional differentiation of florets by recognizing HaNDUA2 in sunflower. Plant Cell Rep 41, 1025–1041 (2022). https://doi.org/10.1007/s00299-022-02835-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-022-02835-4