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The dynamics of sugars, hormones, and cell wall epitopes dictate early somatic embryogenesis in passion fruit (Passiflora edulis Sims)

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Abstract

Sugars, hormones and plant cell wall components regulate many aspects of somatic embryogenesis which requires detailed investigations of the process. In the present study, we investigated the histology, chemical composition of the cell wall, sugar and nitrogen metabolism, and hormonal profile associated with the induction and formation of embryogenic calluses in Passiflora edulis Sims. Zygotic embryos were cultured in induction medium supplemented with 72.4 µM dichlorophenoxyacetic acid and 4.4 µM 6-benzyladenine for 30 days. The zygotic embryo consisted of a uniseriate protoderm and an undifferentiated mesophyll. After 20 days, globular-stage somatic embryos were observed at the periphery of embryogenic calluses. During callus formation, the cell wall of dividing cells showed high levels of methyl-esterified homogalacturonan (HGs) epitopes, recognized for JIM7 antibody. Epitopes of heteromannans (LM21) were identified only in the initial explants, whereas epitopes of xyloglucans (LM15) appeared throughout the morphogenetic process. Cells undergoing transdifferentiation in embryogenic calluses exhibited a drop in epitopes recognized for JIM7 and LM15 and absence of JIM5 labeling. Lipids and proteins were metabolized during early somatic embryogenesis. In contrast, hexose, starch, and amino acid concentrations increased. Hormonal dynamics were also altered: while indole-3-acetic acid and cytokinins decreased during the embryogenic process, jasmonic acid and ethylene showed the opposite trend, indicating a possible role of these stress hormones in the early somatic embryogenesis of passion fruit. These results shed light on the structural and physiological aspects of passion fruit somatic embryogenesis which may help optimize regeneration via somatic embryogenesis of this important commercial passion fruit species.

Key message

The early somatic embryogenesis of passion fruit is mediated by dynamic of sugars and nitrogen metabolism, hormones and cell wall epitopes.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Fundação de Amparo à Pesquisa do Estado de Minas Gerais and the Universidade Federal de Jataí (UFJ) for financial support. The Viveiro Flora Brasil Ltda (Araguari, MG, Brazil) for kindly providing the seeds used in this study, the Editage (www.editage.com) for English language editing and the Rede Mineira de Biotecnologia em Multiplicação e Clonagem de Plantas.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasília, Brazil; Grant No. 420913/2018-1; 311282/2021-0; 303691/2022-0; 310937/2022-1), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasília, Brazil; Grant No. 001), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Belo Horizonte, Brazil; Grant No. APQ-02581-21; RED-00225-23).

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DIR and WCO conceived and designed research. LASS and LLLD conducted experiments. LMV contributed to analysis of the hormonal profile. ANN and MM contributed to biochemical analyses. DCO LLLD, VCK and conducted immunohistochemistry evaluations. DIR, LLLD and MLS analyzed data. DIR, LLLD, VCK and WCO wrote the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Wagner Campos Otoni or Diego Ismael Rocha.

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All the authors declare that there is no conflict of interest. WCO is one of the Associate Editors of the journal. As such he was fully excluded during all the evaluation period of this work, had no access to its handling during peer-refereeing, and his status had no bearing on the editorial consideration of the manuscript.

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Communicated by Sergey V Dolgov.

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Dias, L.L.L., Silva, L.A.S., Vieira, L.M. et al. The dynamics of sugars, hormones, and cell wall epitopes dictate early somatic embryogenesis in passion fruit (Passiflora edulis Sims). Plant Cell Tiss Organ Cult 157, 20 (2024). https://doi.org/10.1007/s11240-024-02733-5

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