cla-miR164-NO APICAL MERISTEM (ClNAM) regulates the inflorescence architecture development of Chrysanthemum lavandulifolium

Junzhuo Li , Xiaohui Wen , Qiuling Zhang , Yuankai Tian , Ya Pu , Jiaying Wang , Bo Liu , Yihan Du , Silan Dai

Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) : 039

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) :039 DOI: 10.1093/hr/uhae039
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cla-miR164-NO APICAL MERISTEM (ClNAM) regulates the inflorescence architecture development of Chrysanthemum lavandulifolium
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Abstract

Chrysanthemum × morifolium has great ornamental and economic value on account of its exquisite capitulum. However, previous studies have mainly focused on the corolla morphology of the capitulum. Such an approach cannot explain the variable inflorescence architecture of the chrysanthemum. Previous research from our group has shown that NO APICAL MERISTEM (ClNAM) is likely to function as a hub gene in capitulum architecture in the early development stage. In the present study, ClNAM was used to investigate the function of these boundary genes in the capitulum architecture of Chrysanthemum lavandulifolium, a closely related species of C. × morifolium in the genus. Modification of ClNAM in C. lavandulifolium resulted in an advanced initiation of the floral primordium at the capitulum. As a result, the receptacle morphology was altered and the number of florets decreased. The ray floret corolla was shortened, but the disc floret was elongated. The number of capitula increased significantly, arranged in more densely compounded corymbose synflorescences. The yeast and luciferase reporter system revealed that ClAP1, ClRCD2, and ClLBD18 target and activate ClNAM. Subsequently, ClNAM targets and activates ClCUC2a/c, which regulates the initiation of floral and inflorescence in C. lavandulifolium. ClNAM was also targeted and cleaved by cla-miR164 in this process. In conclusion, this study established a boundary gene regulatory network with cla-miR164-ClNAM as the hub. This network not only influences the architecture of capitulum, but also affects compound corymbose synflorescences of the C. lavandulifolium. These results provide new insights into the mechanisms regulating inflorescence architecture in chrysanthemum.

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Junzhuo Li, Xiaohui Wen, Qiuling Zhang, Yuankai Tian, Ya Pu, Jiaying Wang, Bo Liu, Yihan Du, Silan Dai. cla-miR164-NO APICAL MERISTEM (ClNAM) regulates the inflorescence architecture development of Chrysanthemum lavandulifolium. Horticulture Research, 2024, 11 (4) : 039 DOI:10.1093/hr/uhae039

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Acknowledgments

This work was supported by National Natural Science Foundation of China (No.32371948, No. 31530064, and No. 31471907).

Author contributions

S.D, J.L, and X.W. conceived the study. J.L and X.W completed the main work. Q.Z. and Y.P. analysed the data. Y.T., J.W., B.L., and Y.D. contributed to planting material and phenotype data observation. J.L. completed the first draft. S.D. and X.W. revised the manuscript. All authors read and approved the final manuscript.

Date availability

Raw sequence data were submitted to the Sequence Read Archive (SRA) database of the National Center for Biotechnology Information (NCBI) (accession number: PRJNA956717).

Conflict of interest statement:

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Broholm SK, Pöllänen E, Ruokolainen S. et al. Functional characterization of B class MADS-box transcription factors in Gerbera hybrida. J Exp Bot. 2010; 61:75-85

[2]

Elomaa P, Zhao Y, Zhang T. Flower heads in Asteraceae—recruitment of conserved developmental regulators to control the flower-like inflorescence architecture. Hort Res. 2018; 5:36

[3]

Sasaki K, Yoshioka S, Aida R. et al. Production of petaloid phenotype in the reproductive organs of compound flowerheads by the co-suppression of class-C genes in hexaploid Chrysanthemum morifolium. Planta. 2021; 253:1-16

[4]

Broholm SK, Tähtiharju S, Laitinen RA. et al. A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. PNAS. 2008; 105:9117-22

[5]

Tähtiharju S, Rijpkema AS, Vetterli A. et al. Evolution and diversification of the CYC/TB1 gene family in Asteraceae—a comparative study in gerbera (Mutisieae) and sunflower (Heliantheae). Mol Biol Evol. 2012; 29:1155-66

[6]

Juntheikki-Palovaara I, Tähtiharju S, Lan T. et al. Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida.(Asteraceae). Plant J. 2014; 79:783-96

[7]

Wen X, Qi S, Huang H. et al. The expression and interactions of ABCE-class and CYC2-like genes in the capitulum development of Chrysanthemum lavandulifolium and C. × morifolium. Plant Growth Regul. 2019; 88:205-14

[8]

Huang D, Li X, Sun M. et al. Identification and characterization of CYC-like genes in regulation of ray floret development in Chrysanthemum morifolium. Front Plant Sci. 2016; 7:1633

[9]

Zhang CJ, Rong YL, Jiang CK. et al. Co-option of a carotenoid cleavage dioxygenase gene (CCD4a) into the floral symmetry gene regulatory network contributes to the polymorphic floral shape-color combinations in Chrysanthemum sensu lato. New Phytol. 2022; 236:1197-211

[10]

Wen X, Qi S, Yang L. et al. Expression pattern of candidate genes in early capitulum morphogenesis of Chrysanthemum lavandulifolium. Sci Hortic. 2019; 252:332-41

[11]

Pu Y, Huang H, Wen X. et al. Comprehensive transcriptomic analysis provides new insights into the mechanism of ray floret morphogenesis in chrysanthemum. Genomics. 2020; 21:1-16

[12]

Wen X, Li J, Wang L. et al. The Chrysanthemum lavandulifolium genome and the molecular mechanism underlying diverse capitulum types. Hort Res. 2022; 9:uhab022

[13]

Souer E, van Houwelingen A, Kloos D. et al. The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell. 1996; 85:159-70

[14]

Žádníková P, Simon R. How boundaries control plant development. Curr Opin Plant Biol. 2014; 17:116-25

[15]

Shuai B, Reynaga-Pena CG, Springer PS. The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol. 2002; 129:747-61

[16]

Cheng X, Peng J, Ma J. et al. NO APICAL MERISTEM (MtNAM) regulates floral organ identity and lateral organ separation in Medicago truncatula. New Phytol. 2012; 195:71-84

[17]

Jiao K, Li X, Guo Y. et al. Regulation of compound leaf development in mungbean (Vigna radiata L.) by CUP-SHAPED COTYLEDON/NO APICAL MERISTEM (CUC/NAM) gene. Planta. 2019; 249:765-74

[18]

Hendelman A, Stav R, Zemach H. et al. The tomato NAC transcription factor SlNAM2 is involved in flower-boundary morphogenesis. J Exp Bot. 2013; 64:5497-507

[19]

Shan T, Fu R, Xie Y. et al. Regulatory mechanism of maize (Zea mays L.) miR164 in salt stress response. Russ J Genet. 2020; 56:835-42

[20]

Chang Z, Xu R, Xun Q. et al. OsmiR164-targeted OsNAM, a boundary gene, plays important roles in rice leaf and panicle development. Plant J. 2021; 106:41-55

[21]

Wang J, Bao J, Zhou B. et al. The Osa-miR164 target OsCUC1 functions redundantly with OsCUC3 in controlling rice meristem/organ boundary specification. New Phytol. 2021; 229:1566-81

[22]

Weir I, Lu J, Cook H. et al. CUPULIFORMIS establishes lateral organ boundaries in antirrhinum. Development. 2004; 131:915-22

[23]

Aida M, Tasaka M. Genetic control of shoot organ boundaries. Curr Opin Plant Biol. 2006; 9:72-7

[24]

Li J, Guo G, Guo W. et al. miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol. 2012; 24:1-14

[25]

Theißen G, Melzer R, Rümpler F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development. 2016; 143:3259-71

[26]

Li J, Zhang Q, Kong D. et al. Genome-wide identification of the MIKCc-type MADS-box gene family in Chrysanthemum lavandulifolium reveals their roles in the capitulum development. Front Plant Sci. 2023; 14:1100

[27]

Guo HS, Xie Q, Fei JF. et al. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell. 2005; 17:1376-86

[28]

Mallory AC, Dugas DV, Bartel DP. et al. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol. 2004; 14:1035-46

[29]

Shi M, Hu X, Wei Y. et al. Genome-wide profiling of small RNAs and degradome revealed conserved regulations of miRNAs on auxin-responsive genes during fruit enlargement in peaches. Int J Mol Sci. 2017; 18:2599

[30]

Nikovics K, Blein T, Peaucelle A. et al. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell. 2006; 18:2929-45

[31]

Zhang T, Cieslak M, Owens A. et al. Phyllotactic patterning of gerbera flower heads. PNAS. 2021; 118:e2016304118

[32]

Pu Y, Liao M, Li J. et al. Floral development stage-specific transcriptomic analysis reveals the formation mechanism of different shapes of ray florets in chrysanthemum. Genes. 2023; 14:766

[33]

Song A, Su J, Wang H. et al. Analyses of a chromosome-scale genome assembly reveal the origin and evolution of cultivated chrysanthemum. Nat Commun. 2023; 14:2021

[34]

Litt A. An evaluation of A-function: evidence from the APETALA1 and APETALA2 gene lineages. Int J Plant Sci. 2007; 168:73-91

[35]

Han Y, Zhang C, Yang H. et al. Cytokinin pathway mediates APETALA1 function in the establishment of determinate floral meristems in Arabidopsis. PNAS. 2014; 111:6840-5

[36]

Blümel M, Dally N, Jung C. Flowering time regulation in crops—what did we learn from Arabidopsis? Curr Opin Biotechnol. 2015; 32:121-9

[37]

Rhoades MW, Reinhart BJ, Lim LP. et al. Prediction of plant microRNA targets. Cell. 2002; 110:513-20

[38]

Zhang T, Zhao Y, Juntheikki I. et al. Dissecting functions of SEPALLATA-like MADS box genes in patterning of the pseudanthial inflorescence of Gerbera hybrida. New Phytol. 2017; 216:939-54

[39]

Tian F, Yang DC, Meng YQ. et al. PlantRegMap: charting functional regulatory maps in plants. Nucleic Acids Res. 2020; 48:D1104-13

[40]

Liu BO, Yan J, Li W. et al. Mikania micrantha genome provides insights into the molecular mechanism of rapid growth. Nat Commun. 2020; 11:340

[41]

Badouin H, Gouzy J, Grassa CJ. et al. The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature. 2017; 546:148-52

[42]

Reyes-Chin-Wo S, Wang Z, Yang X. et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun. 2017; 8:14953

[43]

Song C, Liu Y, Song A. et al. The Chrysanthemum nankingense genome provides insights into the evolution and diversification of chrysanthemum flowers and medicinal traits. Mol Plant. 2018; 11:1482-91

[44]

van Lieshout N, van Kaauwen M, Kodde L. et al. De novo whole-genome assembly of Chrysanthemum makinoi, a key wild chrysanthemum. G3 (Bethesda). 2022; 12:jkab358

[45]

Nakano M, Hirakawa H, Fukai E. et al. A chromosome-level genome sequence of Chrysanthemum seticuspe, a model species for hexaploid cultivated chrysanthemum. Commun Biol. 2021; 4:1167

[46]

Chen C, Chen H, Zhang Y. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13:1194-202

[47]

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32:1792-7

[48]

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009; 25:1972-3

[49]

Minh BQ, Schmidt HA, Chernomor O. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[50]

Lu C, Qu J, Deng C. et al. The transcription factor complex CmAP3-CmPI-CmUIF1 modulates carotenoid metabolism by directly regulating carotenogenic gene CmCCD4a-2 in chrysanthemum. Hort Res. 2022; 9:uhac020

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