Abstract
Key message
The Cyperaceae fruit consistency depends on the mesocarp. Seed structure is diverse and related to the evolutionary history of their species. A new storage tissue is described for Cyperaceae.
Abstract
Anatomy and histochemistry of Cyperaceae fruits (including seeds) are poorly known due to their hard, isolating tissues that prevent anatomical techniques. We performed the first, most comprehensive structural diversity characterisation of fruit and seed in Cyperaceae, accompanied by an unprecedented histochemical characterisation of seeds for this family. We analysed fruits of 29 species, included in 19 genera and 12 tribes within the subfamilies Cyperoideae and Mapanioideae, using light microscopy. Cyperaceae fruits have a pericarp with a one-cell-layered exocarp and endocarp, and a multi-cell-layered mesocarp. The mesocarp of the Mapanioideae has a spongy-fleshy outer region and a hard inner region. The mesocarp of the Cyperoideae has only a hard region. The pericarp is free from the seed coat. Cyperaceae seeds have a three-layered seed coat, an embryo with haustorial function of its scutellum, and two storage tissues: the endosperm and a putative perisperm. Nine seed morphotypes and four seed subtypes were observed among the studied species. Our results suggested that the fruit consistency is determined by the mesocarp. Both the terms “nut” and “achene” should be accepted to refer to the dry fruit of the Cyperaceae until a widely accepted fruit classification for angiosperms is proposed. The Cyperaceae seed structural diversity is high and related to the evolutionary history of the species. The “perisperm” is a new tissue proposed for sedge seeds, and is here characterized for the first time. The seed coat has a different structure than the one described so far for the family.
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References
Allessio Leck M, Schütz W (2005) Regeneration of Cyperaceae, with particular reference to seed ecology and seed banks. Perspect Plant Ecol Evol Syst 7:95–133. https://doi.org/10.1016/j.ppees.2005.05.001
Barroso GM, Morim MP, Peixoto AL, Ichaso CLF (1999) Frutos e sementes: morfologia aplicada à sistemática de dicotiledôneas. Univesidade Federale de Viçosa, Viçosa
Browning J, Gordon-Gray KD, Smith SG (1997) Achene morphology and pericarp anatomy of the type specimens of the Australian and New Zealand Species of Bolboschoenus (Cyperaceae). Aust Syst Bot 10:49–58. https://doi.org/10.1071/SB95039
Bruhl J (1995) Sedge genera of the world: relationships and a new classification. Aust Syst Bot 8:125–305. https://doi.org/10.1071/SB9950125
Coan AI, Alves MV, Scatena VL (2008) Comparative study of ovule and fruit development in species of Hypolytrum and Rhynchospora (Cyperaceae, Poales). Pl Syst Evol 272:181–195. https://doi.org/10.1007/s00606-007-0636-9
Cocucci AE (2005) Morphogenetic seed types of Spermatophyta. Pl Syst Evol 250:1–6. https://doi.org/10.1007/s00606-002-0255-4
Dahlgren RMT, Clifford HT, Yeo PF (1985) The Families of the monocotyledons: structure, evolution, and taxonomy. Springer, Berlin
De Candolle MAP (1813) Théorie élémentaire de la botanique. Déterville, Paris
Denton MF (1983) Anatomical Studies of the Luzulae Group of Cyperus (Cyperaceae). Syst Bot 8:250–262. https://doi.org/10.2307/2418479
Fath A, Bethke P, Lonsdale J, Meza-Romero R, Jones R (2000) Programmed cell death in cereal aleurone. Plant Mol Biol 44:255–266. https://doi.org/10.1023/A:1026584207243
Feder N, O’Brien TP (1968) Plant microtechnique: some principlesand new methods. Am J Bot 55:123–142. https://doi.org/10.1002/j.1537-2197.1968.tb06952.x
Fisher DB (1968) Protein staining of ribboned epon sections for light microscopy. Histochemie 16:92–96. https://doi.org/10.1007/BF00306214
Goetghebeur P (1998) Cyperaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer-Verlag, Berlin, pp 141–190
Goetghebeur P (1986) Genera Cyperacearum. Een bijdrage tot dekennis van de morfologie systematiek en fylogenese van de Cyperaceae-genera. PhD Thesis, Ghent University, Belgium
Gonzalez AM, López MG (2010) Development and morphology of the gynoecium and nutlet in two South American Bulbostylis (Cyperaceae) species. Flora 205:211–220. https://doi.org/10.1016/j.flora.2009.02.002
Hefler SM, Longhi-Wagner HM (2008) Análise da morfologia do fruto em espécies de Cyperus L. subg. Cyperus–Cyperaceae. Acta Bot Bras 22:637–651. https://doi.org/10.1590/S0102-33062008000300005
Jin XF, Zhou YY, Hipp A et al (2014) Nutlet micromorphology of Carex section Rhomboidales sensu Kükenthal (Cyperaceae) and its systematic implications. Bot J Linn Soc 175:123–143. https://doi.org/10.1111/boj.12149
Johansen DA (1940) Plant Microtechnique. McGraw-Hill Book Co, New York
Johnson AM (1931) Taxonomy of the flowering plants. The Century Co, New York
Johri BM, Ambegaokar KB, Srivastava PS (1992) Cyperales. Comparative embryology of angiosperms. Springer-Verlag, Berlin-Heidelberg, pp 974–981
Kern JH (1974) Cyperaceae. In: van Steenis CGGJ (ed) Flora Malesiana I. Noordhoff International Publishing, Leiden, pp 107–187
Khanna P (1965) A contribution to the embryology of Cyperus rotundus L., Scirpus mucrinatus L., and Kyllinga melanospora Nees. Can J Bot 43:1539–1547. https://doi.org/10.1139/b65-163
Larridon I, Zuntini AR, Léveillé-Bourret É et al (2021) A new classification of Cyperaceae (Poales) supported by phylogenomic data. J Syst Evol 59:852–895. https://doi.org/10.1111/jse.12757
López MG, Gonzalez AM (2017) Micromorfología y estructura de los frutos en Bulbostylis (Cyperaceae) y su valor sistemático en las especies de América Austral. Bol Soc Argent Bot 52:69–87. https://doi.org/10.31055/1851.2372.v52.n1.16909
Lye KA (2000) Achene structure and function of structure in Cyperaceae. In: Wilson KL, Morrison DA (eds) Monocots: systematics and evolution. CSIRO, Melbourne, pp 615–628
Lye KA (2016) Chemistry of fruit wall and seed in Cyperaceae tribe Trilepideae. South Afr J Bot 106:104–109. https://doi.org/10.1016/j.sajb.2016.06.003
Makde KH, Bhuskute SM (1984) Trends of specialization in endosperm of the Cyperaceae. Curr Sci 53:504–506
Makde KH, Bhuskute SM (1987) Embryology of Kyllinga monocephala (Cyperaceae) and its systematic position. Pl Syst Evol 156:143–150. https://doi.org/10.1007/BF00936069
Marzinek J, De-Paula OC, Oliveira DMT (2008) Cypsela or achene? Refining terminology by considering anatomical and historical factors. Braz J Bot 31:549–553. https://doi.org/10.1590/S0100-84042008000300018
Masters MT (1871) Classification of fruits. Nature 4(102):6 (Work not seen)
Menapace FJ (1993) Achene micromorphology as a systematic aid to the series placement of Svenson’s undesignated Eleocharis (Cyperaceae) species. Rhodora 95:214–224
Menapace FJ, Wujek DE (1987) The systematic significance of achene micromorphology in Carex retrorsa (Cyperaceae). Brittonia 39:278–283. https://doi.org/10.2307/2807393
Menu MA (1908) Etude Anatomique Du Fruit et la Graine Des Cypéracées. PhD Thèse (Pharm.), Université Paris, France (work not seen)
Munro SL, Linder HP (1997) The embryology and systematic relationships of Prionium serratum (Juncaceae: Juncales). Am J Bot 84:850–860. https://doi.org/10.2307/2445821
Nijalingappa BHM (1977) Post-pollination studies in some Cyperaceae. Proc Indian Acad Sci 85:391–398. https://doi.org/10.1007/BF03052247
Nijalingappa BHM, Palakshaiah CR (1998) Embryological studies in Rhynchospora wightiana (Cyperaceae). In: Shukla AK, Sharma HL (eds) Bela bhatia plant form and function. Angkor Publishers, New Delhi, pp 225–236
O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termacarphi Pty, Melbourne
Padhye MD (1971) Studies in Cyperaceae. III. Life history of Kyllinga brevifolia Rottb. with a brief discussion on systematic position of Kyllinga. Bot Gaz 132:172–179
Prata AP, Thomas WW, Wanderley MG (2008) Micromorfologia da superfície do aquênio em Bulbostylis Kunth (Cyperaceae). Braz J Bot 31:587–596. https://doi.org/10.1590/S0100-84042008000400005
Price RA, Palmer JD (1993) Phylogenetic relationships of the geraniaceae and geraniales from rbcL sequence comparisons. Ann Mo Bot Gard 80:661–671. https://doi.org/10.2307/2399852
Radford WE (1986) Fundamentals of plant systematics. Harper & Row, New York
Ragonese AM, Guaglianone RE, Dizeo de Strittmatter C (1984) Desarrollo del pericarpio con cuerpos de sílice de dos especies de Rhynchospora Vahl (Cyperaceae). Darwiniana 25:27–41
Reutemann AG, Muchut SE, Uberti-Manassero NG et al (2022) A comparative approach to understanding the ovule, seed, and fruit development in Bulbostylis (Cyperaceae: Cyperoideae: Abildgaardieae). Protoplasma 259:141–153. https://doi.org/10.1007/s00709-021-01649-7
Rudall PJ (1997) The nucellus and chalaza in monocotyledons: structure and systematics. Bot Rev 63:140–181. https://doi.org/10.1007/BF02935930
Rudall PJ, Furness CA (1997) Systematics of Acorus: ovule and anther. Int J Plant Sci 158:640–651. https://doi.org/10.1086/297477
Ruzin SE (1999) Plant Microtechnique and microscopy. Oxford University Press, New York
Schneider M (1932) Untersuchungen über die Embryobildung und -entwicklung der Cyperaceen. Beih Zum Botanischen Cent 49:649–674
Schuyler AE (1971) Scanning electron microscopy of achene epidermis in species of Scirpus (Cyperaceae) and related genera. Proc Acad Nat Sci Phila 123:29–52
Semmouri I, Bauters K, Léveillé-Bourret É, Starr JR, Goetghebeur P, Larridon I (2019) Phylogeny and systematics of cyperaceae, the evolution and importance of embryo morphology. Bot Rev 85:1–39. https://doi.org/10.1007/s12229-018-9202-0
Shah CK (1965) Embryogeny in some Cyperaceae. Phytomorphology 15:1–9
Shah CK (1967) A taxonomical evaluation of the families Cyperaceae and Juncaceae. Nat Inst Sci India 38:248–256
Shamrov II (2005) Perisperm. In: Batygina TB (ed) Embryology of flowering plants: terminology and concepts, vol 2. Seed. Science Publishers, Enfield-Plymouth, pp 169–170
Spjut RW (1994) A systematic treatment of fruit types. New York Botanical Garden, New York
Spjut RW (2015) A systematic treatment of fruit types. Web Page. Accessed 10 November 2022. http://www.worldbotanical.com/fruit_types.htm#Overview
Standley LA (1990) Anatomical aspects of the taxonomy of sedges (Carex, Cyperaceae). Can J Bot 68:1449–1456. https://doi.org/10.1139/b90-183
Steedman HF (1950) Alcian Blue 8GS: a new stain for mucin. J Cell Sci 91:477–479. https://doi.org/10.1242/jcs.s3-91.16.477
Strong MT (2006) Taxonomy and distribution of Rhynchospora (Cyperaceae) in the Guianas, South America. Contrib United States Natl Herb 53:1–225
Tejavathi DH (1987) Seed development in some members of Cyperaceae. Beitr Biol Pflanzen 62:43–55
Tiwari DK (1967) Embryological studies in the Cyperaceae. J Indian Bot Soc 47:264–271
Toivonen H, Timonen T (1976) Perigynium and achene epidermis in some species of Carex, subg. Vignea (Cyperaceae), studied by scanning electron microscopy. Ann Bot Fennici 13:49–59
Tucker GC, Miller NG (1990) Achene microstructure in Eriophorum (Cyperaceae): Taxonomic implications and paleobotanical applications. Bull Torrey Bot Club 117:266–283. https://doi.org/10.2307/2996695
Untawale AG, Makde KH (1984) A contribution to the embryology of Scirpus roylei Nees. J Indian Bot Soc 63:298–305
Van der Veken P (1965) Contribution a l’embryographie systématique des Cyperaceae-Cyperoideae. Bull Jard Bot État Brux 35:285–354
Vanhecke L (1974) Embryography of some genera of the Cladiinae and the Gahniinae (Cyperaceae) with additional notes on their fruit anatomy. Bull Jard Bot Belg 44:367–400. https://doi.org/10.2307/3667678
Venning FD (1953) Manual of advanced plant microtechnique. Brown Company Publishers, Dubuque
Wujek DE, Menapace FJ (1986) Taxonomy of Carex section Folliculatae using achene morphology. Rhodora 88:399–403
Wujek DE, Nijalingappa BHM, Garlitz SM (1994) Achene micromorphology of some Indian Cyperaceae II Fimbristylis. Asian J Plant Sci 6:1–17
Zanne AE, Chapman CA, Kitajima K (2005) Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs. Am J Bot 92:972–978. https://doi.org/10.3732/ajb.92.6.972
Acknowledgements
This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica, Argentina (PICT 2019-01678 to A.R.), the Consejo Nacional de Investigaciones Científicas y Técnicas (PIBAA 2022-2023-28720210100408CO01 to A.R.), and the Universidad Nacional del Litoral, Santa Fe, Argentina (CAI+D 2020-50520190100078LI to A.R.). We thank to the staff of Escuela Agrotécnica Pascual Gentilini (Misiones, Argentina), to the staff of Estancia Moat (Tierra del Fuego, Argentina), to the “Fundación Vida Silvestre Argentina”, and to Gastón Rodríguez of “Reserva Ecológica Municipal Ribera Norte” (Buenos Aires, Argentina) for their assistance during plant collection. We also thank Marcelo Moreno (Instituto de Botánica Darwinion) for assistance with Figs. 9 and 10.
Funding
This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica, Argentina (PICT 2019-01678 to A.R.), the Consejo Nacional de Investigaciones Científicas y Técnicas (PIBAA 2022-2023-28720210100408CO01 to A.R.), and the Universidad Nacional del Litoral, Santa Fe, Argentina (CAI+D2020-50520190100078LI to A.R.).
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AGR and REP conceived and designed research. AGR procured funding. AGR and JSM conducted experiments. JSM contributed new reagents and histochemistry techniques. All authors collected samples in the field, and analysed data. AGR wrote the manuscript, and prepared figures. REP and JSM co-wrote and edited the manuscript. All authors read and approved the manuscript.
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Reutemann, A.G., San Martin, J.A.B. & Pozner, R.E. Structural and histochemical approach to the fruit and seed diversity of Cyperaceae in an evolutionary context. Plant Reprod (2023). https://doi.org/10.1007/s00497-023-00465-8
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DOI: https://doi.org/10.1007/s00497-023-00465-8