Skip to main content
SpringerLink
Log in

A pentaploid endosperm and a Penaea-type embryo sac are likely synapomorphies of Azorella (Apiaceae, Azorelloideae)

  • Research
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

About 80% of angiosperms form a monosporic Polygonum-type embryo sac, whereas in the remaining species, eleven other types of embryo sac are found. Evidence as to the type of embryo sac is lacking for many plant species, and the role of higher-ploidy endosperm is unknown. In contrast to the rest of the Apiaceae, where a Polygonum-type embryo sac (3n endosperm) has been reported, the few species of the Azorelloideae studied to form a Drusa-type embryo sac (3n endosperm) or a Penaea-type embryo sac (5n endosperm). This variation within Azorelloideae makes this subfamily, and its genus Azorella in particular, a good candidate for studying the evolutionary importance of the embryo sac and endosperm in diversification. We studied the variation in the type of embryo sac and the ploidy level of the endosperm in Andean-Patagonian Azorella and closely related Pozoa on a sample of 101 individuals from 31 populations of 21 species. We employed flow cytometric seed screening and calibrated the results of ploidy level estimation against embryological observations. In addition, we examined the genome size variation of the species sampled. All species of Azorella formed Penaea-type embryo sacs and a pentaploid endosperm, whereas one species of Pozoa formed triploid and the other tetraploid endosperms. Variations in the type of embryo sac and endosperm ploidy have probably shaped the evolution of the different lineages of Azorelloideae in the southern Andes. A Penaea-type embryo sac, which represents a likely synapomorphy of Azorella, is a feature of underestimated significance in the evolution of angiosperms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersson L, Kocsis M, Eriksson R (2006) Relationships of the genus Azorella (Apiaceae) and other hydrocotyloids inferred from sequence variation in three plastid markers. Taxon 55:270–280. https://doi.org/10.2307/25065577

    Article  Google Scholar 

  • Baroux C, Spillane C, Grossniklaus U (2002) Evolutionary origins of the endosperm in flowering plants. Genome Biol 3:1–5

    Article  Google Scholar 

  • Bell CR, Constance L (1957) Chromosome numbers in Umbelliferae. Amer J Bot 44:565–572. https://doi.org/10.2307/2438928

    Article  Google Scholar 

  • Benton MJ, Wilf P, Sauquet H (2022) The Angiosperm Terrestrial Revolution and the origins of modern biodiversity. New Phytol 233:2017–2035. https://doi.org/10.1111/nph.17822

    Article  Google Scholar 

  • Calviño CI, Fernández M, Martínez SG (2016) Las Especies de Azorella (Azorelloideae, Apiaceae) con distribució extra-Argentina. Darwiniana 4:57–82. https://doi.org/10.14522/darwiniana.2016.41.681

  • Caparelli KF, Peruzzi L, Cesca G (2006) A comparative analysis of embryo-sac development in three closely-related Gagea species (Liliaceae), with some considerations on their reproductive strategies. Pl Biosyst 140:115–122

    Article  Google Scholar 

  • Carputo D, Monti L, Werner JE, Frusciante L (1999) Uses and usefulness of endosperm balance number. Theor Appl Genet 98:478–484. https://doi.org/10.1007/s001220051095

    Article  Google Scholar 

  • Constance L, Chuang T, Bell CR (1971) Chromosome numbers in Umbelliferae. IV. Amer J Bot 58:577–587. https://doi.org/10.1002/j.1537-2197.1971.tb10007.x

    Article  Google Scholar 

  • Constance L, Chuang T, Bell CR (1976) Chromosome numbers in Umbelliferae. V. Amer J Bot 63:608–625. https://doi.org/10.1002/j.1537-2197.1976.tb11849.x

    Article  Google Scholar 

  • Constance L (1988) Umbelliferae. In: Correa MN (ed) Flora Patagónica. Colección Científica del Instituto Nacional de Tecnología Agropecuaria (INTA), Buenos Aires, pp 310–379

  • D’Amato F (1984) Role of polyploidy in reproductive organs and tissues. In: Johri BM (eds) Embryology of angiosperms. Springer, Berlin, Heidelberg, New York, Tokyo, pp 519–566

    Chapter  Google Scholar 

  • Doležel J, Greilhuber J, Suda J (2007) Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley, Weinheim

    Book  Google Scholar 

  • Donoghue MJ, Scheiner SM (1992) The evolution of endosperm: a phylogenetic account. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman & Hall, New York, pp 356–389

    Google Scholar 

  • Ebert I, Greilhuber J (2005) Developmental switch during embryo sac formation from a bisporic mode to the tetrasporic Fritillaria type in Hyacinthoides vincentina (Hoffmannsegg & Link) Rothm. (Hyacinthaceae). Acta Biol Cracov Bot 47:179–184

    Google Scholar 

  • Fagerlind F (1938) Wo kommen tetrasporische, durch drei Teilungsschritte vollentwickelte Embryosäcke unter den Angiospermen vor? Bot Not 1938:461–498

    Google Scholar 

  • Fernández M, Calviño CI (2019) Nueva clasificación infragenérica de Azorella (Apiaceae, Azorelloideae) y sinopsis del subgénero Andinae. Darwiniana Nueva Ser 7:289–304

    Article  Google Scholar 

  • Fernández M, Ezcurra C, Calviño CI (2016) Morphology, fruit anatomy and taxonomy of the South Andean genus Laretia (Azorelloideae, Apiaceae). Syst Bot 41:807–812. https://doi.org/10.1600/036364416X692370

    Article  Google Scholar 

  • Fernández M, Ezcurra C, Calviño CI (2017a) Molecular phylogenetics and evolution chloroplast and ITS phylogenies to understand the evolutionary history of southern South American Azorella, Laretia and Mulinum (Azorelloideae, Apiaceae). Molec Phylogen Evol 108:1–21. https://doi.org/10.1016/j.ympev.2017.01.016

    Article  CAS  Google Scholar 

  • Fernández M, Ezcurra C, Calviño CI (2017b) Revisión taxonómica del género sudamericano Mulinum (Azorelloideae, Apiaceae). Anales Jard Bot Madrid 74:1–31

    Google Scholar 

  • Fernández M, Ezcurra C, Calviño CI (2017c) Species limits and morphometric and environmental variation within the South Andean and Patagonian Mulinum spinosum species-group (Apiaceae-Azorelloideae). Syst Biodivers 15:489–505. https://doi.org/10.1080/14772000.2016.1273975

    Article  Google Scholar 

  • Fernandez M, Martínez SG, Calviño CI (2020) Typifications of 31 names in Azorella (Azorelloideae Apiaceae) from South America. Phytotaxa 433:135–144. https://doi.org/10.11646/phytotaxa.433.2.4

  • Friedman WE (1998) The evolution of double fertilization and endosperm: an” historical” perspective. Sexual Pl Reprod 11:6–16

    Article  Google Scholar 

  • Friedman WE, Madrid EN, Williams JH (2008) Origin of the fittest and survival of the fittest: relating female gametophyte development to endosperm genetics. Int J Pl Sci 169:79–92. https://doi.org/10.1086/523354

    Article  Google Scholar 

  • Haig D (1990) New perspectives on the angiosperm female gametophyte. Bot Rev 56:236–274. https://doi.org/10.1007/BF02858326

    Article  Google Scholar 

  • Håkansson A (1923) Studienüber die Entwicklungsgeschichite der Umbelliferae. Acta Univ Lund 18:1–120

    Google Scholar 

  • Håkansson A (1927) Der sechzehnkernige Embryosack von Azorella trifurcata Gaertn. Hook Ber Deutsch Bot Ges 45:654–664

    Google Scholar 

  • Håkansson A (1952) Seed development in Bowlesia tenera. Bot Not 1:33–45

    Google Scholar 

  • Härdling R, Nilsson P (2001) A model of triploid endosperm evolution driven by parent-offspring conflict. Oikos 92:417–423. https://doi.org/10.1034/j.1600-0706.2001.920303.x

    Article  Google Scholar 

  • Henwood MJ, Hart JM (2001) Towards an understanding of the phylogenetic relationships of Australian Hydrocotyloideae (Apiaceae). Edinburgh J Bot 58:269–289

    Article  Google Scholar 

  • Hojsgaard D, Hörandl E (2015) Apomixis as a facilitator of range expansion and diversification in plants. In: Pontarotti P (ed) Evolutionary biology: biodiversification from genotype to phenotype. Springer, Cham, pp 305–327

    Chapter  Google Scholar 

  • Hörandl E (2006) The complex causality of geographical parthenogenesis. New Phytol 171:525–538. https://doi.org/10.1111/j.1469-8137.2006.01769.x

    Article  Google Scholar 

  • Jurica HS (1922) A morphological study of the Umbelliferae. Bot Gaz 74:292–307

    Article  Google Scholar 

  • Kaushal P, Dwivedi KK, Radhakrishna A et al (2019) Partitioning apomixis components to understand and utilize gametophytic apomixis. Frontiers Pl Sci 10:256

    Article  Google Scholar 

  • Kordyum EL, Mosyakin SL (2020) Endosperm of angiosperms and genomic imprinting. Life 10:1–20

    Article  Google Scholar 

  • Krahulcová A, Rotreklová O (2010) Use of flow cytometry in research on apomictic plants. Preslia 82:23–39

    Google Scholar 

  • López P, Tremetsberger K, Kohl G, Stuessy T (2011) Progenitor–derivative speciation in Pozoa (Apiaceae, Azorelloideae) of the southern Andes. Ann Bot (Oxford) 109:351–363. https://doi.org/10.1093/aob/mcr291

    Article  CAS  Google Scholar 

  • Maheshwari P (1937) A critical review of the types of embryo sacs in angiosperms. New Phytol 36:359–417

    Article  Google Scholar 

  • Martinez S (1989) El género Azorella (Apiaceae-Hydrocotyloideae) en la Argentina. Darwiniana 1:139–178

    Google Scholar 

  • Martínez SG, Calviño CI (2019) Apiaceae. In: Zuloaga FO, Belgrano MJ (eds) Flora Vascular de la República Argentina 20 (2). Talleres Trama S.A., Buenos Aires, pp 1–122

  • Matzk F, Meister A, Schubert I (2000) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Pl J 21:97–108. https://doi.org/10.1046/j.1365-313x.2000.00647.x

    Article  CAS  Google Scholar 

  • Moore DM (1981) Chromosome numbers of Fuegian angiosperms. Bol Soc Brot 53:995–1012

    Google Scholar 

  • Nicolas AN, Plunkett GM (2009) The demise of subfamily Hydrocotyloideae (Apiaceae) and the re-alignment of its genera across the entire order Apiales. Molec Phylogen Evol 53:134–151. https://doi.org/10.1016/j.ympev.2009.06.010

    Article  CAS  Google Scholar 

  • Nicolas AN, Plunkett GM (2012) Untangling generic limits in Azorella, Laretia, and Mulinum (Apiaceae: Azorelloideae): insights from phylogenetics and biogeography. Taxon 61:826–840. https://doi.org/10.1002/tax.614008

    Article  Google Scholar 

  • Nuñez CI, Aizen MA, Ezcurra C (1999) Species associations and nurse plant effects in patches of high-Andean vegetation. J Veg Sci 10:357–364. https://doi.org/10.2307/3237064

    Article  Google Scholar 

  • Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. Methods Cell Biol 33:105–110

    Article  CAS  Google Scholar 

  • Plunkett GM, Nicolas AN (2017) Assessing Azorella (Apiaceae) and its allies: phylogenetics and a new classification. Brittonia 69:31–61. https://doi.org/10.1007/s12228-016-9446-0

    Article  Google Scholar 

  • Rangan P (2020) Endosperm variability: from endoreduplication within a seed to higher ploidy across species, and its competence. Seed Sci Res 30:173–185

    Article  CAS  Google Scholar 

  • Simpson BB, Todzia CA (1990) Patterns and processes in the development of the high Andean flora. Amer J Bot 77:1419–1432. https://doi.org/10.1002/j.1537-2197.1990.tb12552.x

    Article  Google Scholar 

  • Sklenář P (2009) Presence of cushion plants increases community diversity in the high equatorial Andes. Flora-Morphology, Distrib, Funct Ecol Pl 204:270–277

    Google Scholar 

  • Sklenář P, Dušková E, Balslev H (2011) Tropical and temperate: evolutionary history of páramo flora. Bot Rev 77:71–108. https://doi.org/10.1007/s12229-010-9061-9

    Article  Google Scholar 

  • Soltis DE, Albert VA, Leebens-Mack J et al (2009) Polyploidy and angiosperm diversification. Amer J Bot 96:336–348

    Article  Google Scholar 

  • Stephens EL (1909) The embryo-sac and embryo of certain Penaeaceae. Ann Bot (Oxford) 23:363–378

    Article  Google Scholar 

  • Subba Rao AM (1937) A note on the development of the female gametophyte of some Malpighiaceae and polyembryony in Hiptage madablota. Curr Sci 6:280–282

    Google Scholar 

  • Temsch EM, Koutecký P, Urfus T et al (2021) Reference standards for flow cytometric estimation of absolute nuclear DNA content in plants. Cytometry Part A 9:710–724. https://doi.org/10.1002/cyto.a.24495

    Article  Google Scholar 

  • Testolin R, Attorre F, Borchardt P et al (2021) Global patterns and drivers of alpine plant species richness. Global Ecol Biogeogr 30:1218–1231

    Article  Google Scholar 

  • Tseng CC (1967) Anatomical studies of flower and fruit in the Hydrocotyloideae (Umbelliferae). University of California Press, Berkeley

  • Tucker MR, Araujo A-CG, Paech NA et al (2003) Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Pl Cell 15:1524–1537. https://doi.org/10.1105/tpc.011742

    Article  CAS  Google Scholar 

  • Virkki N (1962) Meiosis and Development of the Embryo Sac in Gunnera insignis (Oersted) DC (Halorhagaceae). J Agric Univ Puerto Rico 46:254–268

    Google Scholar 

  • Wilkinson HP, Wanntorp L (2007) Gunneraceae. In: Kubitzki K (ed) Flowering Plants·Eudicots. Springer, Heidelberg, pp 177–183

    Google Scholar 

  • Williams JH, Friedman WE (2002) Identification of diploid endosperm in an early angiosperm lineage. Nature 415:522–526. https://doi.org/10.1038/415522a

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Lenka Macková, Veronika Konečná, Katya Romoleroux, Romina Vidal-Russell for their assistance. Fred Rooks kindly improved the English. The necessary research permit was issued by the Ministerio del Ambiente, Ecuador (No. MAE-DNB-CM-2018-0082), the Ministerio de medio ambiente y agua, Bolivia (No. 026/09) and the Administración de Parque Nacionales, Argentina (No. 1621).

Funding

This work was supported by the Grant Agency of the Czech Republic (project No. 17-12420S), the Grant Agency of Charles University (project No. 1554218) and the following institutions in Argentina: Agencia Nacional de Promoción Científica y Tecnológica PICT 2019-007700, CONICET PIP 112-201301-00357 and Universidad Nacional del Comahue PIN B205.

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Science, Charles University, Benátská 2, 12800, Prague, Czechia

    Jan Ptáček, Petr Sklenář, Jan Pinc, Romana Urfusová & Tomáš Urfus

  2. Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), CONICET – Universidad del Comahue, Quintral 1250, 8400, Bariloche, Rio Negro, Argentina

    Carolina I. Calviño

Authors
  1. Jan Ptáček
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petr Sklenář
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Pinc
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Romana Urfusová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carolina I. Calviño
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tomáš Urfus
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Carolina I. Calviño, Petr Sklenář and Tomáš Urfus conceived the ideas; Jan Ptáček, Petr Sklenář, Tomáš Urfus and Carolina I. Calviño collected the samples; Jan Ptáček, Tomáš Urfus, Romana Urfusová and Jan Pinc performed the laboratory measurements; Carolina I. Calviño determined the species; and Jan Ptáček analysed the data and led the writing of this article with assistance from Carolina I. Calviño, Petr Sklenář and Tomáš Urfus.

Corresponding author

Correspondence to Tomáš Urfus.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Karol Marhold.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 753 KB)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Sampling locations of Azorelloideae species.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ptáček, J., Sklenář, P., Pinc, J. et al. A pentaploid endosperm and a Penaea-type embryo sac are likely synapomorphies of Azorella (Apiaceae, Azorelloideae). Plant Syst Evol 308, 40 (2022). https://doi.org/10.1007/s00606-022-01833-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00606-022-01833-z

Keywords

Search

Navigation