Genome-wide association study (GWAS) analyses of early anatomical changes in rose adventitious root formation.
Rosa × hybrida
Association mapping
Genome-wide association study
Histology
Phloem
Rooting
Xylem
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
23 10 2024
23 10 2024
Historique:
received:
03
04
2024
accepted:
07
10
2024
medline:
24
10
2024
pubmed:
24
10
2024
entrez:
24
10
2024
Statut:
epublish
Résumé
Adventitious root (AR) formation is a genetically complex trait with high genotypic variability. Therefore, only a limited range of cultivars are currently propagated by cuttings in rose. In this study, we analysed the anatomy of in vitro shoots, the early formation of root primordia (RP) and the formation of ARs in a diverse set of 106 rose genotypes. Correlation analysis indicated that the growth in shoot diameter and the vasculature dimensions after 1 week of rooting contributed to successful AR formation. Using phenotypic data for genome-wide association studies (GWAS) analyses, nine significantly associated single nucleotide polymorphisms (SNPs) and genomic regions contributing to various RP and AR formation traits were identified. The contribution of genomic regions to trait variation was notably greater for traits associated with earlier processes than for traits associated with later developmental stages. The combination of RP and AR data allowed the detection of regions by GWAS that contain factors that potentially limit RP emergence. Homologues of 47 genes known to be involved in AR formation from the literature could be assigned to the identified peaks. Further studies are needed to investigate the suitability of SNPs exhibiting strong effects as allele-specific PCR markers for use in breeding.
Identifiants
pubmed: 39443540
doi: 10.1038/s41598-024-75502-1
pii: 10.1038/s41598-024-75502-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25072Informations de copyright
© 2024. The Author(s).
Références
International Association of Horticultural Producers. The International Statistics Flowers & Plants Yearbook 2023 (2023).
Smulders, M. J. M. et al. In the name of the rose: A roadmap for rose research in the genome era. Hortic. Res. 6, 65 (2019).
doi: 10.1038/s41438-019-0156-0
pubmed: 31069087
pmcid: 6499834
Bendahmane, M., Dubois, A., Raymond, O. & Le Bris, M. Genetics and genomics of flower initiation and development in roses. J. Exp. Bot. 64, 847–857 (2013).
doi: 10.1093/jxb/ers387
pubmed: 23364936
pmcid: 3594942
Debener, T. & Linde, M. Exploring complex ornamental genomes: The rose as a model plant. Crit. Rev. Plant Sci. 28, 267–280 (2009).
doi: 10.1080/07352680903035481
Costa, J. M., Heuvelink, E. & van de Pol, P. Propagation by cutting. In Reference Module in Life Sciences (ed. Roitberg, B. D.) https://doi.org/10.1016/B978-0-12-809633-8.05091-3 (Elsevier, 2017).
van de Pol, P. A. & Breukelaar, A. Stenting of roses; a method for quick propagation by simultaneously cutting and grafting. Sci. Hortic. 17, 187–196 (1982).
doi: 10.1016/0304-4238(82)90012-7
Pemberton, H. B. & Karlik, J. F. A recent history of changing trends in USA garden rose plant sales, types, and production methods. Acta Hortic., 223–234 (2015).
Wamhoff, D., Patzer, L., Schulz, D. F., Debener, T. & Winkelmann, T. GWAS of adventitious root formation in roses identifies a putative phosphoinositide phosphatase (SAC9) for marker-assisted selection. PLoS ONE 18, e0287452 (2023).
doi: 10.1371/journal.pone.0287452
pubmed: 37595005
pmcid: 10437954
Wamhoff, D., Schulz, D., Debener, T. & Winkelmann, T. Genome-wide association study and marker development for adventitious root formation in rose. Acta Hortic. 331–340 (2023).
Nguyen, T. H. N., Tänzer, S., Rudeck, J., Winkelmann, T. & Debener, T. Genetic analysis of adventitious root formation in vivo and in vitro in a diversity panel of roses. Sci. Hortic. 266, 109277 (2020).
doi: 10.1016/j.scienta.2020.109277
Druege, U. et al. Molecular and physiological control of adventitious rooting in cuttings: Phytohormone action meets resource allocation. Ann. Bot. 123, 929–949 (2019).
doi: 10.1093/aob/mcy234
pubmed: 30759178
pmcid: 6589513
Bellini, C., Pacurar, D. I. & Perrone, I. Adventitious roots and lateral roots: Similarities and differences. Annu. Rev. Plant Biol. 65, 639–666 (2014).
doi: 10.1146/annurev-arplant-050213-035645
pubmed: 24555710
Morales-Orellana, R. J., Winkelmann, T., Bettin, A. & Rath, T. Stimulation of adventitious root formation by laser wounding in rose cuttings: A matter of energy and pattern. Front. Plant Sci. 13, 1009085 (2022).
doi: 10.3389/fpls.2022.1009085
pubmed: 36247617
pmcid: 9557736
Druege, U., Franken, P. & Hajirezaei, M. R. Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front. Plant Sci. 7, 186360 (2016).
doi: 10.3389/fpls.2016.00381
De Klerk, G.-J., van der Krieken, W. & De Jong, J. C. Review the formation of adventitious roots: New concepts, new possibilities. In Vitro Cell. Dev. Biol. Plant 35, 189–199 (1999).
doi: 10.1007/s11627-999-0076-z
da Costa, C. T. et al. When stress and development go hand in hand: Main hormonal controls of adventitious rooting in cuttings. Front. Plant Sci. 4, 45174 (2013).
doi: 10.3389/fpls.2013.00133
Mhimdi, M. & Pérez-Pérez, J. M. Understanding of adventitious root formation: What can we learn from comparative genetics?. Front. Plant Sci. 11, 582020 (2020).
doi: 10.3389/fpls.2020.582020
pubmed: 33123185
pmcid: 7573222
Yu, Y. et al. Transcriptomic profiles of poplar (Populus simonii × P. nigra) cuttings during adventitious root formation. Front. Genet. 13, 968544 (2022).
Ahkami, A. et al. Comprehensive transcriptome analysis unravels the existence of crucial genes regulating primary metabolism during adventitious root formation in Petunia hybrida. PLoS ONE 9, e100997 (2014).
doi: 10.1371/journal.pone.0100997
pubmed: 24978694
pmcid: 4076263
Dokane, K., Megre, D., Lazdane, M. & Kondratovics, U. Does shoot anatomical heterogeneity influence ex vitro adventitious root formation in rhododendron microcuttings. Propag. Ornam. Plants 14, 171–176 (2014).
Syros, T., Yupsanis, T., Zafiriadis, H. & Economou, A. Activity and isoforms of peroxidases, lignin and anatomy, during adventitious rooting in cuttings of Ebenus cretica L. J. Plant Physiol. 161, 69–77 (2004).
doi: 10.1078/0176-1617-00938
pubmed: 15002666
Koning-Boucoiran, C. F. S. et al. Using RNA-Seq to assemble a rose transcriptome with more than 13,000 full-length expressed genes and to develop the WagRhSNP 68k Axiom SNP array for rose (Rosa L.). Front. Plant Sci. 6, 249 (2015).
Hibrand Saint-Oyant, L. et al. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat. Plants 4, 473–484 (2018).
Cheng, C.-Y. et al. Araport11: A complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 89, 789–804 (2017).
doi: 10.1111/tpj.13415
pubmed: 27862469
Rosyara, U. R., Jong, W. S. de, Douches, D. S. & Endelman, J. B. Software for genome-wide association studies in autopolyploids and its application to potato. Plant Genome 9 (2016).
Guan, L. et al. Physiological and molecular regulation of adventitious root formation. Crit. Rev. Plant Sci. 34, 506–521 (2015).
doi: 10.1080/07352689.2015.1090831
Li, S.-W. Molecular bases for the regulation of adventitious root generation in plants. Front. Plant Sci. 12, 614072 (2021).
doi: 10.3389/fpls.2021.614072
pubmed: 33584771
pmcid: 7876083
Dubois, L. A. & Vries, D. P. de. Variation in adventitious root formation of softwood cuttings of Rosa chinensis minima (Sims) Voss cultivars. Sci. Hortic. 47, 345–349 (1991).
Pei, H. et al. An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiol. 163, 775–791 (2013).
doi: 10.1104/pp.113.223388
pubmed: 23933991
pmcid: 3793057
Ilegems, M. et al. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137, 975–984 (2010).
doi: 10.1242/dev.047662
pubmed: 20179097
Qu, Y. et al. Transcriptional regulation of Arabidopsis copper amine oxidase ζ (CuAOζ) in indole-3-butyric acid-induced lateral root development. Plant Growth Regul. 89, 287–297 (2019).
doi: 10.1007/s10725-019-00535-w
Fabre, G. et al. The ABCG transporter PEC1/ABCG32 is required for the formation of the developing leaf cuticle in Arabidopsis. New Phytol. 209, 192–201 (2016).
doi: 10.1111/nph.13608
pubmed: 26406899
Ito, H. & Gray, W. M. A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol. 142, 63–74 (2006).
doi: 10.1104/pp.106.084533
pubmed: 16877699
pmcid: 1557603
Xu, L. et al. Abnormal inflorescence meristem1 functions in salicylic acid biosynthesis to maintain proper reactive oxygen species levels for root meristem activity in rice. Plant Cell 29, 560–574 (2017).
doi: 10.1105/tpc.16.00665
pubmed: 28298519
pmcid: 5385951
Dong, C.-J., Liu, X.-Y., Xie, L.-L., Wang, L.-L. & Shang, Q.-M. Salicylic acid regulates adventitious root formation via competitive inhibition of the auxin conjugation enzyme CsGH3.5 in cucumber hypocotyls. Planta 252, 75 (2020).
Rawat, R. et al. Reveille1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc. Natl. Acad. Sci. USA 106, 16883–16888 (2009).
doi: 10.1073/pnas.0813035106
pubmed: 19805390
pmcid: 2757846
Gil, P. et al. BIG: A calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985–1997 (2001).
doi: 10.1101/gad.905201
pubmed: 11485992
pmcid: 312751
Huang, T. et al. Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell 26, 246–262 (2014).
doi: 10.1105/tpc.113.111526
pubmed: 24464295
pmcid: 3963573
Gerth, K. et al. Guilt by association: A phenotype-based view of the plant phosphoinositide network. Annu. Rev. Plant Biol. 68, 349–374 (2017).
doi: 10.1146/annurev-arplant-042916-041022
pubmed: 28125287
Schulz, D. F. et al. Genome-wide association analysis of the anthocyanin and carotenoid contents of rose petals. Front. Plant Sci. 7, 1798 (2016).
doi: 10.3389/fpls.2016.01798
pubmed: 27999579
pmcid: 5138216
Nguyen, T. H. N., Schulz, D., Winkelmann, T. & Debener, T. Genetic dissection of adventitious shoot regeneration in roses by employing genome-wide association studies. Plant Cell Rep. 36, 1493–1505 (2017).
doi: 10.1007/s00299-017-2170-8
pubmed: 28647832
Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473–497 (1962).
doi: 10.1111/j.1399-3054.1962.tb08052.x
Nicolazzi, E. L., Iamartino, D. & Williams, J. L. AffyPipe: An open-source pipeline for affymetrix axiom genotyping workflow. Bioinformatics 30, 3118–3119 (2014).
doi: 10.1093/bioinformatics/btu486
pubmed: 25028724
pmcid: 4609010
Voorrips, R. & Gort, G. fitTetra: fitTetra is an R package for assigning tetraploid genotype (2013).
Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
doi: 10.1093/bioinformatics/btn129
pubmed: 18397895
Wickham, H. ggplot2. Elegant Graphics for Data Analysis. 2nd ed (Springer, 2016).
Hahsler, M. & Nagar, A. rBLAST: R Interface for the Basic Local Alignment Search Tool (2019).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021).
Wei, T. & Simko, V. R package ‘corrplot’: Visualization of a Correlation Matrix (2021).
Lenth, R. V. emmeans: Estimated Marginal Means, aka Least-Squares Means (2022).