Unveiling the phenology and associated floral regulatory pathways of Humulus lupulus L. in subtropical conditions.
FLOWERING LOCUS T (HlFT)
TERMINAL FLOWER (HlTFL)
Development
Hop MicroRNA156/172
Hop flowering
Photoperiod
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
10 May 2024
10 May 2024
Historique:
received:
24
11
2023
accepted:
01
05
2024
medline:
10
5
2024
pubmed:
10
5
2024
entrez:
10
5
2024
Statut:
epublish
Résumé
The hop phenological cycle was described in subtropical condition of Brazil showing that flowering can happen at any time of year and this was related to developmental molecular pathways. Hops are traditionally produced in temperate regions, as it was believed that vernalization was necessary for flowering. Nevertheless, recent studies have revealed the potential for hops to flower in tropical and subtropical climates. In this work, we observed that hops in the subtropical climate of Minas Gerais, Brazil grow and flower multiple times throughout the year, independently of the season, contrasting with what happens in temperate regions. This could be due to the photoperiod consistently being inductive, with daylight hours below the described threshold (16.5 h critical). We observed that when the plants reached 7-9 nodes, the leaves began to transition from heart-shaped to trilobed-shaped, which could be indicative of the juvenile to adult transition. This could be related to the fact that the 5th node (in plants with 10 nodes) had the highest expression of miR156, while two miR172s increased in the 20th node (in plants with 25 nodes). Hop flowers appeared later, in the 25th or 28th nodes, and the expression of HlFT3 and HlFT5 was upregulated in plants between 15 and 20 nodes, while the expression of HlTFL3 was upregulated in plants with 20 nodes. These results indicate the role of axillary meristem age in regulating this process and suggest that the florigenic signal should be maintained until the hop plants bloom. In addition, it is possible that the expression of TFL is not sufficient to inhibit flowering in these conditions and promote branching. These findings suggest that the reproductive transition in hop under inductive photoperiodic conditions could occur in plants between 15 and 20 nodes. Our study sheds light on the intricate molecular mechanisms underlying hop floral development, paving the way for potential advancements in hop production on a global scale.
Identifiants
pubmed: 38727772
doi: 10.1007/s00425-024-04428-9
pii: 10.1007/s00425-024-04428-9
doi:
Substances chimiques
MicroRNAs
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
150Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 149043/2019-8
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Acosta A, Rechcigl J, Bollin S et al (2021) Hop (“Humulus lupulus” L.) phenology, growth, and yield under subtropical climatic conditions: effects of cultivars and crop management. Aust J Crop Sci 15:764–772. https://doi.org/10.3316/informit.167653807817601
doi: 10.3316/informit.167653807817601
Adrian J, Farrona S, Reimer JJ et al (2010) cis-regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22:1425–1440. https://doi.org/10.1105/tpc.110.074682
doi: 10.1105/tpc.110.074682
pubmed: 20472817
pmcid: 2899882
Ahn JH, Miller D, Winter VJ et al (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614. https://doi.org/10.1038/sj.emboj.7600950
doi: 10.1038/sj.emboj.7600950
pubmed: 16424903
pmcid: 1383534
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402
doi: 10.1093/nar/25.17.3389
pubmed: 9254694
pmcid: 146917
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-Like target genes. Plant Cell 15:2730–2741. https://doi.org/10.1105/tpc.016238
doi: 10.1105/tpc.016238
pubmed: 14555699
pmcid: 280575
Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769. https://doi.org/10.1105/tpc.107.051706
doi: 10.1105/tpc.107.051706
pubmed: 17601824
pmcid: 1955733
Bauerle WL (2019) Disentangling photoperiod from hop vernalization and dormancy for global production and speed breeding. Sci Rep 9:1–8. https://doi.org/10.1038/s41598-019-52548-0
doi: 10.1038/s41598-019-52548-0
Cardon CH, de Oliveira RR, Lesy V et al (2022) Expression of coffee florigen CaFT1 reveals a sustained floral induction window associated with asynchronous flowering in tropical perennials. Plant Sci 325:111479. https://doi.org/10.1016/j.plantsci.2022.111479
doi: 10.1016/j.plantsci.2022.111479
pubmed: 36181945
Cardoso TCdS, Alves TC, Caneschi CM et al (2018) New insights into tomato microRNAs. Sci Rep 8:16069. https://doi.org/10.1038/s41598-018-34202-3
doi: 10.1038/s41598-018-34202-3
pubmed: 30375421
pmcid: 6207730
Castillejo C, Pelaz S (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr Biol 18:1338–1343. https://doi.org/10.1016/j.cub.2008.07.075
doi: 10.1016/j.cub.2008.07.075
pubmed: 18718758
Cheng Y-J, Shang G-D, Xu Z-G et al (2021) Cell division in the shoot apical meristem is a trigger for miR156 decline and vegetative phase transition in Arabidopsis. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.2115667118
doi: 10.1073/pnas.2115667118
pubmed: 34933999
pmcid: 8719871
Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767–778. https://doi.org/10.1105/tpc.106.049767
doi: 10.1105/tpc.106.049767
pubmed: 17369370
pmcid: 1867375
Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033. https://doi.org/10.1126/science.1141752
doi: 10.1126/science.1141752
pubmed: 17446353
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucl Acids Res 39:W155–W159. https://doi.org/10.1093/nar/gkr319
doi: 10.1093/nar/gkr319
pubmed: 21622958
pmcid: 3125753
Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucl Acids Res 46:W49–W54. https://doi.org/10.1093/nar/gky316
doi: 10.1093/nar/gky316
pubmed: 29718424
pmcid: 6030838
Dantas AAA, de Carvalho LG, Ferreira E (2007) Classificação e tendências climáticas em Lavras, MG. Ciênc E Agrotecnol 31:1862–1866. https://doi.org/10.1590/S1413-70542007000600039
doi: 10.1590/S1413-70542007000600039
de Oliveira RR, Viana AJC, Reátegui ACE, Vincentz MGA (2015) An efficient method for simultaneous extraction of high-quality RNA and DNA from various plant tissues. Genet Mol Res 4:18828–18838
doi: 10.4238/2015.December.28.32
de Souza GM, Muniyappa MK, Carvalho SG et al (2011) Genome-wide identification of novel microRNAs and their target genes in the human parasite Schistosoma mansoni. Genomics 98:96–111. https://doi.org/10.1016/j.ygeno.2011.05.007
doi: 10.1016/j.ygeno.2011.05.007
Dodds K (2017) Hops a guide for new growers. NSW Department of Primary Industries
Fagherazzi MM, Sarnighausen VR, Rufato L et al (2023) Climatological conditions of the southern Santa Catarina state highlands for hop production. Rev Ceres 70:1–7. https://doi.org/10.1590/0034-737X202370040001
doi: 10.1590/0034-737X202370040001
Falavigna VdS, Guitton B, Costes E, Andrés F (2019) I want to (bud) break free: the potential Role of DAM and SVP-like genes in regulating dormancy cycle in temperate fruit trees. Front Plant Sci 9
Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166. https://doi.org/10.1111/j.1096-0031.1989.tb00562.x
doi: 10.1111/j.1096-0031.1989.tb00562.x
Fouracre JP, Poethig RS (2019) Role for the shoot apical meristem in the specification of juvenile leaf identity in Arabidopsis. Proc Natl Acad Sci 116:10168–10177. https://doi.org/10.1073/pnas.1817853116
doi: 10.1073/pnas.1817853116
pubmed: 31023887
pmcid: 6525512
Fric V, Havel J, Libich V et al (1991) Developments in crop science. Elsevier Science Publishers, New York
Ho WWH, Weigel D (2014) Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564. https://doi.org/10.1105/tpc.113.115220
doi: 10.1105/tpc.113.115220
pubmed: 24532592
pmcid: 3967025
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347
Hofacker IL (2003) Vienna RNA secondary structure server. Nucl Acids Res 31:3429–3431. https://doi.org/10.1093/nar/gkg599
doi: 10.1093/nar/gkg599
pubmed: 12824340
pmcid: 169005
Hu H, Tian S, Xie G et al (2021) TEM1 combinatorially binds to FLOWERING LOCUS T and recruits a Polycomb factor to repress the floral transition in Arabidopsis. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.2103895118
doi: 10.1073/pnas.2103895118
pubmed: 34934004
pmcid: 8719886
Huang N-C, Luo K-R, Yu T-S (2018) Mobility of antiflorigen and PEBP mRNAs in tomato-tobacco heterografts. Plant Physiol 178:783–794. https://doi.org/10.1104/pp.18.00725
doi: 10.1104/pp.18.00725
pubmed: 30150303
pmcid: 6181055
Jastrombek JM, Faguerazzi MM, de Cássio PH et al (2022) Hop: an emerging crop in subtropical areas in Brazil. Horticulturae 8:393. https://doi.org/10.3390/horticulturae8050393
doi: 10.3390/horticulturae8050393
Jin S, Nasim Z, Susila H, Ahn JH (2021) Evolution and functional diversification of FLOWERING LOCUS T/TERMINAL FLOWER 1 family genes in plants. Semin Cell Dev Biol 109:20–30. https://doi.org/10.1016/j.semcdb.2020.05.007
doi: 10.1016/j.semcdb.2020.05.007
pubmed: 32507412
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066
doi: 10.1093/nar/gkf436
pubmed: 12136088
pmcid: 135756
Kobayashi Y, Kaya H, Goto K et al (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962. https://doi.org/10.1126/science.286.5446.1960
doi: 10.1126/science.286.5446.1960
pubmed: 10583960
Leles NR, Sato AJ, Rufato L et al (2023) Performance of hop cultivars grown with artificial lighting under subtropical conditions. Plants 12:1971. https://doi.org/10.3390/plants12101971
doi: 10.3390/plants12101971
pubmed: 37653888
pmcid: 10222731
Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
doi: 10.1093/nar/30.1.325
pubmed: 11752327
pmcid: 99092
Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucl Acids Res 49:W293–W296. https://doi.org/10.1093/nar/gkab301
doi: 10.1093/nar/gkab301
pubmed: 33885785
pmcid: 8265157
Liu C, Chen H, Er HL et al (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Dev Camb Engl 135:1481–1491. https://doi.org/10.1242/dev.020255
doi: 10.1242/dev.020255
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
López ME, Silva Santos I, Marquez Gutiérrez R et al (2022) Crosstalk between ethylene and abscisic acid during changes in soil water content reveals a new role for 1-aminocyclopropane-1-carboxylate in coffee anthesis regulation. Front Plant Sci 13:824948
doi: 10.3389/fpls.2022.824948
pubmed: 35463406
pmcid: 9019592
Márquez Gutiérrez R, Cherubino Ribeiro TH, de Oliveira RR et al (2022) Genome-wide analyses of MADS-Box genes in Humulus lupulus L. reveal potential participation in plant development, floral architecture, and lupulin gland metabolism. Plants 11:1237. https://doi.org/10.3390/plants11091237
doi: 10.3390/plants11091237
pubmed: 35567239
pmcid: 9100628
Mathieu J, Yant LJ, Mürdter F et al (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7:e1000148. https://doi.org/10.1371/journal.pbio.1000148
doi: 10.1371/journal.pbio.1000148
pubmed: 19582143
pmcid: 2701598
McGarry RC, Ayre BG (2012) Manipulating plant architecture with members of the CETS gene family. Plant Sci 188–189:71–81. https://doi.org/10.1016/j.plantsci.2012.03.002
doi: 10.1016/j.plantsci.2012.03.002
pubmed: 22525246
Mishra AK, Kocábek T, Sukumari Nath V et al (2020) Dissection of dynamic transcriptome landscape of leaf, bract, and lupulin gland in hop (Humulus lupulus L.). Int J Mol Sci 21:233. https://doi.org/10.3390/ijms21010233
doi: 10.3390/ijms21010233
Moraes TS, Dornelas MC, Martinelli AP (2019) FT/TFL1: calibrating plant architecture. Front Plant Sci 10:97. https://doi.org/10.3389/fpls.2019.00097
doi: 10.3389/fpls.2019.00097
pubmed: 30815003
pmcid: 6381015
Natsume S, Takagi H, Shiraishi A et al (2015) The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol 56:428–441. https://doi.org/10.1093/pcp/pcu169
doi: 10.1093/pcp/pcu169
pubmed: 25416290
Padgitt-Cobb LK, Kingan SB, Wells J et al (2021) A draft phased assembly of the diploid Cascade hop (Humulus lupulus) genome. Plant Genome 14:e20072. https://doi.org/10.1002/tpg2.20072
doi: 10.1002/tpg2.20072
pubmed: 33605092
Patzak J, Henychová A (2018) Evaluation of genetic variability within actual hop (Humulus lupulus L.) cultivars by an enlarged set of molecular markers. Czech J Genet Plant Breed 54:86–91. https://doi.org/10.17221/175/2016-CJGPB
doi: 10.17221/175/2016-CJGPB
Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35:1742–1755. https://doi.org/10.1111/j.1365-3040.2012.02558.x
doi: 10.1111/j.1365-3040.2012.02558.x
pubmed: 22697796
Roßbauer G, Buhr L, Hack H et al (1995) Phänologische Entwicklungsstadien von Kultur-Hopfen (Humulus lupulus L.) Codierung und Beschreibung nach der erweiterten BBCH-Skala mit Abbildungen. Nachr Dtsch Pflanzenschutzd 47:249–249
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
doi: 10.1093/oxfordjournals.molbev.a040454
pubmed: 3447015
Schwab R (2012) The roles of miR156 and miR172 in phase change regulation. In: Sunkar R (ed) MicroRNAs in plant development and stress responses. Springer, Berlin, pp 49–68
doi: 10.1007/978-3-642-27384-1_3
Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucl Acids Res 43:W7–W14. https://doi.org/10.1093/nar/gkv318
doi: 10.1093/nar/gkv318
pubmed: 25883146
pmcid: 4489236
Shephard HL, Parker JS, Darby P, Ainsworth CC (2000) Sexual development and sex chromosomes in hop. New Phytol 148:397–411. https://doi.org/10.1046/j.1469-8137.2000.00771.x
doi: 10.1046/j.1469-8137.2000.00771.x
pubmed: 33863027
Silva PO, Batista DS, Cavalcanti JHF et al (2019) Leaf heteroblasty in Passiflora edulis as revealed by metabolic profiling and expression analyses of the microRNAs miR156 and miR172. Ann Bot 123:1191–1203. https://doi.org/10.1093/aob/mcz025
doi: 10.1093/aob/mcz025
pubmed: 30861065
pmcid: 6612941
Steibel JP, Poletto R, Coussens PM, Rosa GJM (2009) A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94:146–152. https://doi.org/10.1016/j.ygeno.2009.04.008
doi: 10.1016/j.ygeno.2009.04.008
pubmed: 19422910
Tamaki S, Matsuo S, Wong HL et al (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036. https://doi.org/10.1126/science.1141753
doi: 10.1126/science.1141753
pubmed: 17446351
Teotia S, Tang G (2015) To bloom or not to bloom: role of MicroRNAs in plant flowering. Mol Plant 8:359–377. https://doi.org/10.1016/j.molp.2014.12.018
doi: 10.1016/j.molp.2014.12.018
pubmed: 25737467
Thomas GG, Schwabe WW (1969) Factors controlling flowering in the hop (Humulus lupulus L.). Ann Bot 33:781–793
doi: 10.1093/oxfordjournals.aob.a084324
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192. https://doi.org/10.1093/bib/bbs017
doi: 10.1093/bib/bbs017
pubmed: 22517427
Vander Schoor JK, Hecht V, Aubert G et al (2022) Defining the components of the miRNA156-SPL-miR172 aging pathway in pea and their expression relative to changes in leaf morphology. Plant Gene 30:100354. https://doi.org/10.1016/j.plgene.2022.100354
doi: 10.1016/j.plgene.2022.100354
Varkonyi-Gasic E, Wu R, Wood M et al (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12. https://doi.org/10.1186/1746-4811-3-12
doi: 10.1186/1746-4811-3-12
pubmed: 17931426
pmcid: 2225395
Verzele M, Keukeleire DD (1991) Chemistry and analysis of hop and beer bitter acids. Elsevier B.V, Oxford
Wang J-W (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4723–4730. https://doi.org/10.1093/jxb/eru246
doi: 10.1093/jxb/eru246
pubmed: 24958896
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8:983–997. https://doi.org/10.1016/j.molp.2015.01.007
doi: 10.1016/j.molp.2015.01.007
pubmed: 25598141
Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759. https://doi.org/10.1016/j.cell.2009.06.031
doi: 10.1016/j.cell.2009.06.031
pubmed: 19703400
pmcid: 2732587
Yamaguchi A, Kobayashi Y, Goto K et al (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189. https://doi.org/10.1093/pcp/pci151
doi: 10.1093/pcp/pci151
pubmed: 15951566
Yant L, Mathieu J, Dinh TT et al (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170. https://doi.org/10.1105/tpc.110.075606
doi: 10.1105/tpc.110.075606
pubmed: 20675573
pmcid: 2929098
Zheng J, Ma Y, Zhang M et al (2019) Expression pattern of FT/TFL1 and miR156-targeted SPL genes associated with developmental stages in Dendrobium catenatum. Int J Mol Sci 20:2725. https://doi.org/10.3390/ijms20112725
doi: 10.3390/ijms20112725
pubmed: 31163611
pmcid: 6600168
Zhu D, Rosa S, Dean C (2015) Nuclear organization changes and the epigenetic silencing of FLC during vernalization. J Mol Biol 427:659–669. https://doi.org/10.1016/j.jmb.2014.08.025
doi: 10.1016/j.jmb.2014.08.025
pubmed: 25180639
Zhu Y, Klasfeld S, Jeong CW et al (2020) TERMINAL FLOWER 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat Commun 11:5118. https://doi.org/10.1038/s41467-020-18782-1
doi: 10.1038/s41467-020-18782-1
pubmed: 33046692
pmcid: 7550357