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Unveiling the phenology and associated floral regulatory pathways of Humulus lupulus L. in subtropical conditions

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Abstract

Main conclusion

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.

Abstract

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.

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Data availability

Main data supporting the findings of this study are available within the paper and its supplementary materials published online. The raw data used for analyses and figures are available from the corresponding author, Antonio Chalfun-Júnior, upon request.

Abbreviations

NB:

Northern Brewer

miRNAs:

MicroRNAs

SAM:

Shoot apical meristem

AP2:

APETALA2

SPL:

SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE family

FT :

FLOWERING LOCUS T

TFL1 :

TERMINAL FLOWER 1

RT-qPCR:

Real-time quantitative PCR

PEBP:

PHOSPHATIDYLETHANOLAMINE-BINDING PROTEIN

References

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Acknowledgements

The authors thank the Universidade Federal de Lavras (UFLA/Brazil) and members of the Laboratório de Fisiologia Molecular de Plantas (LFMP, UFLA/Brazil) for the structural support of the experiments and analysis; we also thank to Jane Fátima da Silva to support in the field. The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). R.M.G. received a PhD scholarship from the PAEC-OAS-GCUB-Program—Organization of American States and CNPq (grant 149043/2019-8).

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Authors and Affiliations

Authors

Contributions

RRO, RMG, and AC-J conceptualized the project; RMG conducted all data research and analyses; THCR supported the bioinformatic analyses; RRO and AC-J supervised the experiments and analyses KKPO supported in the molecular analyses; JVNS, TCA, LRdA, MdSG, and MdSG contributed to the miRNAs prediction; RMG wrote the first version of the manuscript and RRO contributed to final version writing; all the co-authors corrected and contributed to the writing of the final manuscript version.

Corresponding author

Correspondence to Antonio Chalfun-Junior.

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Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Communicated by De-Yu Xie.

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Supplementary Information

Below is the link to the electronic supplementary material.

425_2024_4428_MOESM1_ESM.tif

Alignment of miR156 precursors showing the 5’ and 3’ arms in the sequences (A). The hairpin structure formed by the eight miR156 precursors of hop (B) (TIF 1955 KB)

425_2024_4428_MOESM2_ESM.tif

Alignment of miR172 precursors showing the 5’ and 3’ arms in the sequences (A). Hairpin structure that formed by the four miR172 precursors of hop (B) (TIF 1467 KB)

425_2024_4428_MOESM3_ESM.tif

Cis-regulatory elements predicted in positive and negative strands of 6000 nt upstream of translation start site of FT-likes genes and HlTFL3 (TIF 2354 KB)

Supplementary file4 (DOCX 28 KB)

Supplementary file5 (DOCX 16 KB)

Sequences of primers used for RT-qPCR analyses (XLSX 10 KB)

Family of microRNAs identified in the hop genome (XLSX 27 KB)

Localization of eight miR156 and four miR172 in the hop genome (XLSX 9 KB)

425_2024_4428_MOESM9_ESM.xlsx

Targets of mature sequences of miR 156 and 172, expectation, start and end, alignment with the mRNA of targets, inhibition way, and domains identified in the targets (XLSX 9 KB)

PEBP genes identified in hop cascade genome (XLSX 9 KB)

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Gutiérrez, R.M., de Oliveira, R.R., Ribeiro, T.H.C. et al. Unveiling the phenology and associated floral regulatory pathways of Humulus lupulus L. in subtropical conditions. Planta 259, 150 (2024). https://doi.org/10.1007/s00425-024-04428-9

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  • DOI: https://doi.org/10.1007/s00425-024-04428-9

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