Karyotype alterations, meiotic abnormalities, and reduced pollen viability in triploid cytotypes of Passiflora foetida (Passifloraceae) derived from endosperm cultures

Joelson Oliveira Barros; Lyderson Facio Viccini; Elyabe Monteiro Matos; Wagner Campos Otoni; Aryane Campos Reis; Saulo Marçal Sousa; Diego Ismael Rocha; Maurecilne Lemes Silva

doi:10.1590/2447-536X.v31.e312797

Authors

Joelson Oliveira Barros Universidade do Estado de Mato Grosso https://orcid.org/0000-0003-2348-8590
Lyderson Facio Viccini Universidade Federal de Juiz de Fora https://orcid.org/0000-0002-7575-8241
Elyabe Monteiro Matos Universidade Federal de Juiz de Fora https://orcid.org/0000-0002-3466-4927
Wagner Campos Otoni Universidade Federal de Viçosa https://orcid.org/0000-0002-9614-9373
Aryane Campos Reis Universidade Federal de Juiz de Fora https://orcid.org/0000-0002-2419-9996
Saulo Marçal Sousa Universidade Federal de Juiz de Fora https://orcid.org/0000-0001-8229-9330
Diego Ismael Rocha Universidade Federal de Viçosa https://orcid.org/0000-0001-6683-0961
Maurecilne Lemes Silva Universidade do Estado de Mato Grosso https://orcid.org/0000-0001-6928-285X

DOI:

https://doi.org/10.1590/2447-536X.v31.e312797

Keywords:

chromosome banding, heterochromatin, meiotic behavior, passion fruit, triploids

Abstract

The polyploidy induction offers the possibility to generate new variations in plant shape, color, fragrance, form, shelf life, flower architecture, and adaptability to adverse environments. Considering the importance of such information for understanding the effects of triploidy and homologous diploid on the reproductive biology of this cytotype of Passiflora foetida. To better understand the effects of triploidy on the reproductive biology of Passiflora foetida, this study aimed to compare the karyotype, meiotic behavior, and pollen viability of diploid and triploid cytotypes. Karyotyping, heterochromatin patterns, meiosis, and pollen viability assessments were conducted using differential DAPI and chromomycin A3 (CMA3) staining. As expected, diploid plants exhibited normal meiotic behavior, with approximately 75% viable pollen, whereas triploid cytotypes displayed abnormalities in both meiotic divisions and had approximately 70% unviable pollen. Despite these irregularities, triploid cytotypes demonstrated greater chromosomal stability in somatic cells compared to diploids. Given that chromosomal behavior plays a key role in reproduction and fertility, these findings provide valuable insights for breeding strategies and the development of improved P. foetida cultivars with desirable traits.

Downloads

Download data is not yet available.

References

AFONSO, A.; LOUREIRO, J.; ARROYO, J.; VICENTE, E.O.; CASTRO, S. Cytogenetic diversity in the polyploid complex Linum suffruticosum s.l. (Linaceae). Botanical Journal of the Linnean Society, v.195, p.216- 232, 2021. https://doi.org/10.1093/botlinnean/boaa060

ALEXANDER, L. Ploidy level influences pollen tube growth and seed viability in interploidy crosses of Hydrangea macrophylla. Frontiers in Plant Science, v.11, p.100, 2020. https://doi.org/10.3389/fpls.2020.00100

ANTONIAZZI, C.A.; FARIA, R.B.; CARVALHO, P.P.; MIKOVSKI, A.I.; CARVALHO, I.F.; MATOS, E.M.; REIS, A.C.; VICCINI, L.F.; PAIM PINTO, D.L.; ROCHA, D.I.; OTONI, W.C.; SILVA, M.L. In vitro regeneration of triploid plants from mature endosperm culture of commercial passionfruit (Passiflora edulis Sims). Science Horticulture, Science Horticulture, v.238, p.408-415, 2018. https://doi.org/10.1016/j.scienta.2018.05.001

ASKURA, I.; HOSHINO, Y. Endosperm-derived triploid plant regeneration in diploid Actinidia kolomikta, a cold-hardy kiwifruit relative. Scientia Horticulturae, v.219, p.53-59, 2017. https://doi.org/10.1016/j.scienta.2017.02.045

BARTOLIĆ, P.; VOLTROVA A.; MACKOVA, L.; ŠRAMKOVA,G.; ŠLENKER, M.; MANDAKOVA, T.; PADILLA GARCIA, N.; MARHOLD, K.; KOLAŘ, F. Overcoming ploidy barriers: the role of triploid bridges in the genetic introgression of Cardamine amara. Molecular Ecology, v.0, e17702, 2025. https://doi.org/10.1111/mec.17702

BASIT, A.; LIM, K. Systematic approach of polyploidy as an evolutionary genetic and genomic phenomenon in horticultural crops. Plant Science, v.348, p.112236, 2024. https://doi.org/10.1016/j.plantsci.2024.112236

BEGNA, T. Polyploidy’s genetic effects in crop improvement: a review. Middle East Journal of Agriculture Research, v.13, p.137-147, 2024.

BLASIO, F.; PRIETO, P.; PRADILLO, M.; NARANJO, T. Genomic and meiotic changes accompanying polyploidization. Plants, v.11, n.1, p.125, 2022. https://doi.org/10.3390/plants11010125

CARVALHO, C.R.; SARAIVA, L.S. High-resolution HKG-banding in maize mitotic chromosomes. Journal of Plant Research, v.110, p.417- 420, 1997. https://doi.org/10.1007/bf02506801

COMAI, L. The advantages and disadvantages of being polyploid. Nature reviews. Genetics, v.6, p.836–846, 2005. https://doi.org/10.1038/nrg1711

CUI, L.; LIU, Z.; YIN, Y.; ZOU, Y.; FAIZAN, M.; ALAM, P.; YU, F. Research progress of chromosome doubling and 2n gametes of ornamental plants. Horticulturae, v.9, p.752, 2023. https://doi.org/10.3390/horticulturae9070752

FILIPPI, M.; BOLDRINI, K.R.; AGOSTINNHO, K.F.; CORRÊA, S.J.S.; DONAZOLLO, J. Estudo citogenético e viabilidade do pólen de Diatenopteryx sorbifolia Radlk. Ciência Florestal, v.32, n.1, p.233-246, 2022. https://doi.org/10.5902/1980509848072

FORRESTER, N.J.; REBOLLEDA-GÓMEZ, M.; SACHS, J.L.; ASHAMAN, T.L. Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism. New Phytologist, v.227, p.944–954, 2020. https://doi.org/10.1111/nph.16574

HESLOP-HARRISON, J.; HESLOP-HARRISON, Y. Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate. Stain Technology, v.45, p.115-120, 1970. https://doi.org/10.3109/10520297009085351

IANNICELLI, J.; GUARINIELLO, J.; TOSSI, J.J.; REGALADO, L.; DI-CIANCCIO, L.; VAN-BAREN, C.M.; PITTA ALVAREZ, S.I.; ESCANDÓN, A.S. The “polyploid effect” in the breeding of aromatic and medicinal species. Scientia Horticulturae, v.260, p.108854, 2020. https://doi.org/10.1016/j.scienta.2019.108854

ISLAM, M.M.; DEEPO, D.M.; NASIF, S.O.; SIDDIQUE, A.B.; HASSAN, O.; PAUL, N.C. Cytogenetics and consequences of polyploidization on different biotic-abiotic stress tolerance and the potential mechanisms involved. Plants, v.11, p.2684, 2022. https://doi.org/10.3390/plants11202684

JIAO, Y.; WICKETT, N.; AYYAMPALAYAM, S.; CHANDERBALI, A.S.; LANDHERR, L.; RALPH, P.E.; TOMSHO, L.P.; HU, Y.; LIANG, H.; SOLTIS, P.S.; SOLTIS, D.E.; CLIFTON, S.W.; SCHARBAUM, S.E.; SCUSTER, S.C.; MA, H.; LEEBENS-MACK, J.; PAMPHILIS, C.W. Ancestral polyploidy in seed plants angiosperms. Nature, v.473, p.97- 100, 2011. https://doi.org/10.1038/nature09916

JOHRI, B.M.; NAG, K. Cytology and morphogenesis of embryo and endosperm tissues of Dendrophthoe and Taxillus. Cytology, v.39, p.801- 813, 1974. DOI: https://doi.org/10.1508/cytologia.39.801

JULIÃO, S.A.; RIBEIRO, C.V.; LOPES, J.M.L.; MATOS, E.M.; REIS, A.C.; PEIXOTO, P.H.P.; MACHADO, M.A.; AZEVEDO, A.L.S.; GRAZUL, R.M.; CAMPOS, J.M.S.; VICCINI, L.F. Induction of synthetic polyploids and assessment of genomic stability in Lippia alba. Frontiers in Plant Science, v.11, p.292, 2020. https://doi.org/10.3389/fpls.2020.00292

LA COUR, F. Acetic-orcein: a new stain-fixative for chromosomes. Biotechnic & Histochemistry, v.16, p.169-174, 1941.

LIQIN, G.; JIANGUO, Z.; XIAOXIA, L.; GUODONG, R. Polyploidy-related differential gene expression between diploid and synthesized allotriploid and allotetraploid hybrids of Populus. Molecular Breeding, v.39, p.69, 2019. https://doi.org/10.1007/s11032-019-0975-6

MACHADO, M.D.; SOUZA, C.S.; MACHADO, M.; REIS, A.C.; SOUSA, S.M.; MATOS, E.M.; VICCINI, L.F.; OTONI, W.C.; CARVALHO, I.F.; ROCHA, D.I.; SILVA, M.L. Novel avenues for passion fruit in vitro regeneration from endosperm culture, and morpho- agronomic and physiological traits of triploid Passiflora cincinnata Mast. emblings. Plant Cell Tissue Organ Culture, v.150, p.637-650, 2022. https://doi.org/10.1007/s11240-022-02318-0

MIKOVSKI, A.I.; SILVA, N.T.; SILVA, L.A.S.; MACHADO, M.; BARBOSA, L.C.S.; REIS, A.C.; MATOS, E.M.; VICCINI, L.F.; SOUZA, C.S.; MACHADO, M.D.; OOTONI, W.C.; CARVALHO, I.F.; ROCHA, D.I.; SILVA, M.L. From endosperm to triploid plants: a stepwise characterization of the de novo shoot organogenesis and morpho- agronomic aspects of an ornamental passion fruit (Passiflora foetida L.). Plant Cell Tissue Organ Culture, v.147, p.239-253, 2021. https://doi.org/10.1007/s11240-021-02120-4

MOHAMED, M.E.; HICKS, R.G.T.; BLAKESLEY, D. Shoot regeneration from mature endosperm of Passiflora foetida. Plant Cell Tissue Organ Culture, v.46, p.161-164, 1996. DOI: https://doi.org/10.1007/BF00034851

MURASHIGE, T.; SKOOG, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, v.15, p.473–497, 1962. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

NIAZIAN, M.; NALOUSI, A.M. Artificial polyploidy induction for improvement of ornamental and medicinal plants. Plant Cell Tissue Organ Culture, v.142, p.447-469, 2020. https://doi.org/10.1007/s11240-020-01888-1

OTONI, W.C.; SOARES, J.R.; SOUZA, C.S.; SILVA, L.A.S.S.; DIAS, L.L.L.; ROBLEDO, K.J.M.; PAIM-PINTO, D.L.; KOEHLER, A.D.; SODRZEIESKI, P.A.; FERNANDES, A.M.; VIEIRA, L.M.; SILVA, P.O.; SILVEIRA, E.C.; MATOS, E.M.; CARVALHO, I.F.; ROMANEL, E.; BATISTA, D.S.; VICCINI, L.F.; FALEIRO, F.G.; ROCHA, D.I.; NOGUEIRA, F.T.S.; SILVA, M.L.C. Advances in Tissue Culture and Transformation Studies in Non-model Species: Passiflora spp. (Passifloraceae). In: LOYOLA-VARGAS, V.; OCHOA-ALEJO, N. (eds). Plant Cell Protocols. Methods in Molecular Biology, v. 2827,. New York: Humana, 2024. pp.207-222.

SCHWEIZER, D. Reverse fluorescent chromosome-banding with chromomycin A and DAPI. Chromosoma, v.58re, p.307-324, 1976. https://doi.org/10.1007/BF00292840

SILVA, M.L.; PINTO, D.L.P.; CAMPOS, J.M.S.; CARVALHO, I.F.; ROCHA, D.I.; BATISTA, D.S.; OTONI, W.C. Repetitive somatic embryogenesis from wild passion fruit (Passiflora cincinnata Mast.) anthers. Plant Cell Tissue Organ Culture, v.146, p.635-641, 2021. https://doi.org/10.1007/s11240-021-02083-6

SILVA, N.T.; FARIA, R.B.; CREPALDI, G.B.; Crepaldi, G.B.; Paim-Pinto, D.L.; Viccini, L.F.; de Matos, E.M.; da Silva, M.L. Karyotype characterization of endosperm-derived plants of Passiflora cristalina Vanderplank and Zappi, a wild amazonian passionfruit species. Plant Cell Tissue Organ Culture, v.156, 102, 2024. https://doi.org/10.1007/s11240-024-02714-8

SILVA, N.T.; SILVA, L.A.S.; REIS, A.C.; MACHADO, M.D.; MATOS, E.M.; VICCINI, L.F.; OTONI, W.C.; CARVALHO, I.F.; ROCHA, D.I.; SILVA, M.L. Endosperm culture: a facile and efficient biotechnological tool to generate passion fruit (Passiflora cincinnata Mast.) triploid plants. Plant Cell Tissue Organ Culture. v.142, p.613-624, 2020. https://doi.org/10.1007/s11240-020-01887-2

SOARES, N.R.; MOLLINARI, M.; OLIVEIRA, G.K.; PEREIRA, G.S.; VIEIRA, M.L.C. Meiosis in polyploids and implications for genetic mapping: a review. Genes, v.12, p.1517, 2021. https://doi.org/10.3390/genes12101517

SOLTIS, P.S.; SOLTIS, D.E. Polyploidy and Genome Evolution. New York: Springer, 2014. 420p.

STEBBINS, G.L. Chromosomal evolution in higher plants. In: G. Ledyard Stebbins (eds.) London: Edward Arnold Ltd., 1971.

SVAČINA, R.; KARAFIÁTOVÁ, M.; MALUROVÁ, M.; SERRA, H.; VITEK, D.; ENDO, T.R.; SOURDILLE, P.; BARTOS, J. Development of deletion lines for chromosome 3D of bread wheat. Frontiers in Plant Science, v.10, 2019. https://doi.org/10.3389/fpls.2019.01756

THOMAS, T.D.; CHATURVEDI, R. Endosperm culture: a novel method for triploid plant production. Plant Cell Tissue and Organ Culture, v.93, p.1-14, 2008. https://doi.org/10.1007/s11240-008-9336-6

TOUCHELL, D.H.; PALMER, I.E., RANNEY, T.G. In vitro ploidy manipulation for crop improvement. Frontiers in Plant Science, v.11, p.722, 2020. https://doi.org/10.3389/fpls.2020.00722

WANG, X.; CHENG, Z.M.; ZHI, S.; XU, F. Breeding Triploid Plants: A Review. Czech Journal of Genetics and Plant Breeding, v.52, p.41-54, 2016. https://doi.org/10.17221/151/2015-CJGPB