Floral morphology and development reveal extreme diversification in some species of Croton (Euphorbiaceae).
Croton
Euphorbiaceae
Floral diversity
Floral morphology
Floral ontogeny
Journal
Journal of plant research
ISSN: 1618-0860
Titre abrégé: J Plant Res
Pays: Japan
ID NLM: 9887853
Informations de publication
Date de publication:
29 Aug 2024
29 Aug 2024
Historique:
received:
12
11
2023
accepted:
15
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
29
8
2024
Statut:
aheadofprint
Résumé
Floral diversity of Croton, the second largest genus in Euphorbiaceae, is currently under-explored. Several clades demonstrate an unusual floral morphology, e.g., lower or higher stamen number, bilateral symmetry and reduced ovary, but have never been investigated in a comparative study with typical Croton. This study examined morphology and ontogeny of flowers in nine Croton species from different clades within the genus with light and scanning microscopy, resin sectioning and micro-computed tomography. In staminate flowers, great variations of stamen number and arrangement are observed. The ancestral androecium likely consisted of two or more whorls with the outermost antepetalous stamen whorl developing centrifugally. Modification by reduction of the antepetalous whorl resulted in an outer alternipetalous stamen whorl in Croton section Moacroton, subgenus Quadrilobi. Several species in the subgenus Geiseleria show an independent reduction of stamen numbers by absence of a centrifugal development with the antepetalous whorl the first whorl to develop. Petal losses are observed in the distantly related C. setiger and C. dioicus. Chaotic stamen arrangement is found in C. celtidifolius (subgenus Adenophylli) as a result of a secondary stamen increase. In pistillate flowers, reduction of carpel numbers happened three times in the subgenus Geiseleria. C. monanthogynus has a bicarpellate ovary, while in C. setiger and C. michauxii the ovary is monocarpellate. Reduction of carpel number is linked with merism change and perianth reduction. The ovary in C. michauxii has basal placentation which is unique among all Croton. Moreover, strong bilateral sepals and nectaries are observed in species from section Julocroton. Therefore, the floral diversity of some species in the genus Croton could be explained by developmental modification of an ancestral form via reduction, rearrangement of stamen whorls, and symmetry shifts.
Identifiants
pubmed: 39207556
doi: 10.1007/s10265-024-01572-x
pii: 10.1007/s10265-024-01572-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s) under exclusive licence to The Botanical Society of Japan.
Références
Alain H (1960) Novedades en la Flora cubana, XIII. Candollea 17:113–121
Baillon H (1858) Etude générale du groupe des Euphorbiacées. V. Masson, Paris
Berry PE, Hipp AL, Wurdack KJ et al (2005) Molecular phylogenetics of the giant genus Croton and tribe Crotoneae (Euphorbiaceae sensu stricto) using ITS and TrnL-TrnF DNA sequence data. Am J Bot 92:1520–1534
doi: 10.3732/ajb.92.9.1520
pubmed: 21646170
Berry PE, Van Ee BW, Kainulainen K, Achtemeier L (2016) Croton cupreolepis (Euphorbiaceae), a new coppery-lepidote tree species from eastern Madagascar. Syst Bot 41:977–982. https://doi.org/10.1600/036364416X694099
doi: 10.1600/036364416X694099
Bhattacharya A, Sukantamajumdar S (2015) Allomorphic female flower in Acalypha indica L.: A case study of heterobathmy and neutral evolution. Chromosome Bot 10:1–5. https://doi.org/10.3199/iscb.10.1
doi: 10.3199/iscb.10.1
Bittrich V, Amaral MCE (1996) Flower morphology and pollination biology of some Clusia species from the Gran Sabana (Venezuela). Kew Bull 51:681. https://doi.org/10.2307/4119722
doi: 10.2307/4119722
Bittrich V, Kühn U (1993) Nyctaginaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants. Volume II Flowering plants. Dicotyledons: Magnoliid, Hamamelid and Acryophyllid Families. Springer
de Sá-Haiad B, Silva CP, Paula RCV et al (2015) Androecia in two Clusia species: development, structure and resin secretion. Plant Biol J 17:816–824. https://doi.org/10.1111/plb.12314
doi: 10.1111/plb.12314
Dehgan B, Webster GL (1979) Morphology and infrageneric relationships of the genus Jatropha Euphorbiaceae. University of California Press
Dehgan B, Schutzman B (1994) Contributions toward a monograph of neotropical Jatropha: Phenetic and phylogenetic analyses. Ann Missouri Bot Garden 81:349. https://doi.org/10.2307/2992102
doi: 10.2307/2992102
Dehgan, (2012) Jatropha (Euphorbiaceae). The New York botanical garden press, New York
De-Paula OC, das Graças Sajo M, Prenner G et al (2011a) Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales). Plant Syst Evol 292:1–14. https://doi.org/10.1007/s00606-010-0388-9
doi: 10.1007/s00606-010-0388-9
De-Paula OC, Sajo M, das G, (2011b) Morphology and development of anthers and ovules in Croton and Astraea (Euphorbiaceae). Nordic J Bot 29:505–511. https://doi.org/10.1111/j.1756-1051.2011.01072.x
doi: 10.1111/j.1756-1051.2011.01072.x
Erbar C (1995) On the floral development of Sphenoclea zeylanica (Sphenocleaceae, Campanulales)—SEM-investigations on herbarium material. Bot Jahrb Syst Pflanzengesch Pflanzengeogr 117:469–483
Esser H-J (2003) Fruit characters in Malesian Euphorbiaceae. Telopea 10:169–177. https://doi.org/10.7751/telopea20035613
doi: 10.7751/telopea20035613
Friis I, Gilbert MG (2008) Croton megalocarpoides sp. nov. an arborescent Euphorbiaceae from semi-evergreen vegetation in S Somalia and E Kenya. Nordic J Bot 4:327–331. https://doi.org/10.1111/j.1756-1051.1984.tb01503.x
doi: 10.1111/j.1756-1051.1984.tb01503.x
Gagliardi KB, Cordeiro I, Demarco D (2017) Flower development in species of Croton (Euphorbiaceae) and its implications for floral morphological diversity in the genus. Aust J Bot 65:538. https://doi.org/10.1071/BT17045
doi: 10.1071/BT17045
Gama T, do SS, Cordeiro I, Demarco D, (2019) Floral structure and development in Alchornea sidifolia (Acalyphoideae) and the evolution of wind pollination in Euphorbiaceae. Brazil J Bot 42:307–317. https://doi.org/10.1007/s40415-019-00535-0
doi: 10.1007/s40415-019-00535-0
Gandhi KN, Thomas RD (1983) A note on the androecium of the genus Croton and flowers in general of the family Euphobiaceae. Phytologia 54:6–8
Govaerts R, Frodin DG, Radcliffe-Smith A (2000) World checklist and bibliography of Euphorbiaceae (and Pandaceae). Royal Botanic Garden Kew, London, 2
Gustafsson MHG (2000) Floral morphology and relationships of Clusia gundlachii with a discussion of floral organ identity and diversity in the genus Clusia. Int J Plant Sci 161:43–53. https://doi.org/10.1086/314229
doi: 10.1086/314229
pubmed: 10648193
Haegens RMAP (2000) Taxonomy, phylogeny, and biogeography of Baccaurea, Distichirhops, and Nothobaccaurea (Euphorbiaceae). Blumea Supplement 12:1–218
Hochwallner H, Weber A (2006) Flower development and anatomy of Clusia valerioi, a central American species of Clusiaceae offering floral resin. Flora - Morphol, Distrib, Funct Ecol Plants 201:407–418. https://doi.org/10.1016/j.flora.2005.07.017
doi: 10.1016/j.flora.2005.07.017
Hoffmann P, Wurdack KJ (2006) Radcliffea, a new genus of Euphorbiaceae sensu stricto from Madagascar. Kew Bull 61:193–197
Katsuhara KR, Kitamura S, Ushimaru A (2017) Functional significance of petals as landing sites in fungus-gnat pollinated flowers of Mitella pauciflora (Saxifragaceae). Funct Ecol 31:1193–1200. https://doi.org/10.1111/1365-2435.12842
doi: 10.1111/1365-2435.12842
Kenoyer LA (1919) Dimorphic carpellate flower of Acalypha indica L. J Indian Bot 1:3–7
Kulju KKM, Sierra SEC, van Welzen PC (2007) Re-shaping Mallotus [Part 2]: inclusion of Neotrewia , Octospermum and Trewia in Mallotus s.s. (Euphorbiaceae s.s.). Blum-J Plant Tax Plant Geog. https://doi.org/10.3767/000651907X612364
doi: 10.3767/000651907X612364
Leon H, Alain H (1953) Flora de Cuba vol III Dicotiledoneas: Malpighiaceae a Myrtaceae. (IM, UK)
Levin GA, Cardinal-McTeague WM, Steinmann VW, Sagun VG (2022) Phylogeny, Classification, and Character Evolution of Acalypha (Euphorbiaceae: Acalyphoideae). Syst Bot 47:477–497. https://doi.org/10.1600/036364422X16512572275034
doi: 10.1600/036364422X16512572275034
Marchand N-L (1861) Du Croton tiglium. Recherches botaniques et thérapeutiques. Faculté de médecine de Paris
Michaelis P (1924) Blütenmorphologische Untersuchungen an den Euphorbiaceen, unter besonderer Berücksichtigung der Phylogenie der Angiospermenblüte. Botanische Abhandlungen 3:1–150
Müller J (1866) Euphorbiaceae. In: Prodomus systematis naturalis regni vegetabilis. Treuttel & Würtz, Paris
Nair NC, Abraham V (1962) Floral morphology of a few species of Euphorbiaceae. Pro Indian Acad Sci Sect B 56:1–12
doi: 10.1007/BF03051524
Okuyama Y, Pellmyr O, Kato M (2008) Parallel floral adaptations to pollination by fungus gnats within the genus Mitella (Saxifragaceae). Mol Phylogenet Evol 46:560–575. https://doi.org/10.1016/j.ympev.2007.09.020
doi: 10.1016/j.ympev.2007.09.020
pubmed: 18248825
Pax F (1896) Euphorbiaceae. In: Die natürlichen Pflanzenfamilien. Verlag von Wilhelm Engelmann, Leipzig
Payer JB (1857) Traité d’organogénie comparée de la fleur. Victor Masson, Paris
Peterson RL, Hersey RE, Brisson JD (1978) Embedding softened herbarium material in spurr’s resin for histological studies. Stain Technol 53:1–9
doi: 10.3109/10520297809111436
pubmed: 78541
Pinto-Silva NP, de Souza KF, Silva OLM, Vitarelli NC, Pereira APN, Soares DA, Sodré RC, Medeiros D, Caruzo MBR, Carneiro Torres DS, da Silva MJ, Meira RMSA, Riina R, Feio AC (2023) Trichomes in the megadiverse genus Croton (Euphorbiaceae): a revised classification, identification parameters and standardized terminology. Bot J Linn Soc 203:37–49. https://doi.org/10.1093/botlinnean/boad008
doi: 10.1093/botlinnean/boad008
Radcliffe-Smith A (1973) Allomorphic female flowers in the genus Acalypha (Euphorbiaceae). Kew Bull 28:525. https://doi.org/10.2307/4108897
doi: 10.2307/4108897
Radcliffe-Smith A (2001) Genera Euphorbiacearum. Royal Botanic Garden Kew
Riina R, Berry PE, van Ee BW (2009) Molecular phylogenetics of the dragon’s blood Croton Section Cyclostigma (Euphorbiaceae): A polyphyletic assemblage unraveled. Syst Bot 34:360–374
doi: 10.1600/036364409788606415
Riina R, Van Ee BW, Caruzo MBR, Carneiro-Torres DS, dos Santos RF, Berry PE (2021) The neotropical Croton sect. Geiseleria (Euphorbiaceae): classification update, phylogenetic framework, and seven new species from South America. Ann Missouri Bot Garden 106:111–166
doi: 10.3417/2021669
Riina R, Cordeiro I, Amorim AM, Berry PE (2010) Croton thomasii Riina & P. E. Berry (Euphorbiaceae), a new species from the Atlantic forest in the state of Bahia (Brazil) and typification of Croton sapiifolius Müll. Arg. Candollea 65:101–107. https://doi.org/10.15553/c2010v651a9
doi: 10.15553/c2010v651a9
Rohwer JG (1993) Phytolaccaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants. Volume II. Flowering plants. Dicotyledons: Magnoliid, Hamamelid and Acryophyllid Families. Springer-Verlag, London, 506–515
Ronse De Craene LP (2021) Gynoecium structure and development in core Caryophyllales: a matter of proportions. Bot J Linn Soc 195:437–466. https://doi.org/10.1093/botlinnean/boaa048
doi: 10.1093/botlinnean/boaa048
Ronse De Craene L, Bull-Hereñu K (2016) Obdiplostemony: the occurrence of a transitional stage linking robust flower configurations. Ann Bot 117:709–724. https://doi.org/10.1093/aob/mcw017
doi: 10.1093/aob/mcw017
pubmed: 27013175
pmcid: 4845804
Ronse De Craene LP, Smets EF (1991) The floral ontogeny of some members of the Phytolaccaceae (subfamily Rivinoideae) with a discussion of the evolution of the androecium in the Rivinoideae. Biol Jb Dodnaea 59:77–99
Ronse De Craene L, Smets E (1995) The distribution and systematic relevance of the androecial character oligomery. Bot J Linn Soc 118:193–247. https://doi.org/10.1016/S0024-4074(05)80002-6
doi: 10.1016/S0024-4074(05)80002-6
Ronse De Craene LP, Stuppy W (2010) Floral development and anatomy of Aextoxicon punctatum (Aextoxicaceae-Berberidopsidales): an enigmatic tree at the base of core eudicots. Int J Plant Sci 171:244–257. https://doi.org/10.1086/650161
doi: 10.1086/650161
Rosendahl CO (1914) A revision of the genus Mitella with a discussion of geographical distribution and relationships. Bot Jahrb Syst 50:357–397
Salatino A, Salatino MLF, Negri G (2007) Traditional uses, chemistry and pharmacology of Croton species (Euphorbiaceae). J Braz Chem Soc 18:11–33. https://doi.org/10.1590/S0103-50532007000100002
doi: 10.1590/S0103-50532007000100002
Sattler R, Perlin L (1982) Floral development of Bougainvillea spectabilis Willd., Boerhaavia diffusa L. and Mirabilis jalapa L. (Nyctaginaceae). Bot J Linn Soc 84:161–182. https://doi.org/10.1111/j.1095-8339.1982.tb00532.x
doi: 10.1111/j.1095-8339.1982.tb00532.x
Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
doi: 10.1038/nmeth.2019
pubmed: 22743772
Secco RDS (2004) Alchorneae (Euphorbiaceae) (Alchornea, Aparisthmium e Conceveiba). Flora Neotropica 93:1–194
Secco RDS, Giulietti AM (2004) Sinopse das espécies de Alchornea (Euphorbiaceae, Acalyphoideae) na Argentina. 18
Sodré RC, Silva MJD (2017) Croton rhodotrichus: A New Species of Croton Section Geiseleria (A. Gray) Baill. (Euphorbiaceae) from the State of Mato Grosso. Brazil Syst Bot 42:338–345. https://doi.org/10.1600/036364417X695600
doi: 10.1600/036364417X695600
Sodré RC, de Souza AO, Alonso AA, da Silva MJ (2019) Molecular, morphological, and anatomical data support a new species of Croton sect. Geiseleria (Crotonoideae, Euphorbiaceae). Plant Syst Evol 305:233–246. https://doi.org/10.1007/s00606-019-1566-z
doi: 10.1007/s00606-019-1566-z
Sokoloff DD, Nuraliev MS, Oskolski AA, Remizowa MV (2017) Gynoecium evolution in angiosperms: Monomery, pseudomonomery, and mixomery. Moscow Univ BiolSci Bull 72:97–108. https://doi.org/10.3103/S0096392517030105
doi: 10.3103/S0096392517030105
Staedler YM, Masson D, Schönenberger J (2013) Plant tissues in 3D via X-Ray tomography: simple contrasting methods allow high resolution imaging. PLoS ONE 8:e75295. https://doi.org/10.1371/journal.pone.0075295
doi: 10.1371/journal.pone.0075295
pubmed: 24086499
pmcid: 3785515
Sutter D, Endress PK (1995) Aspect of gynoecium structure and macrosystematics in Euphorbiaceae. Bot Jahrb Syst Pflanzengesch Pflanzengeogr 116:517–536
Thaowetsuwan P, Ritchie S, Riina R, Ronse De Craene L (2020) Divergent developmental pathways among staminate and pistillate flowers of some unusual Croton (Euphorbiaceae). Front Ecol Evol. https://doi.org/10.3389/fevo.2020.00253
doi: 10.3389/fevo.2020.00253
Tucker SC, Bernhardt P (2000) Floral ontogeny, pattern formation, and evolution in Hibbertia and Adrastaea (Dilleniaceae). Am J Bot 87:1915–1936. https://doi.org/10.2307/2656843
doi: 10.2307/2656843
pubmed: 11118428
van Ee B, Berry PE (2009a) The circumscription of Croton section Crotonopsis (Euphorbiaceae), a North American endemic. Harv Pap Bot 14:61–70. https://doi.org/10.3100/025.014.0110
doi: 10.3100/025.014.0110
van Ee BW, Berry PE (2009b) A phylogenetic and taxonomic review of Croton (Euphorbiaceae S.S.) on Jamaica including the description of Croton jamaicensis, a new species of section Eluteria. Syst Bot 34:129–140
doi: 10.1600/036364409787602203
van Ee BW, Berry PE (2010) Taxonomy and phylogeny of Croton section Heptallon (Euphorbiaceae). Syst Bot 35:151–167
doi: 10.1600/036364410790862461
van Ee BW, Berry PE, Riina R, Amaro JEG (2008) Molecular phylogenetics and biogeography of the Caribbean-Centered Croton subgenus Moacroton (Euphorbiaceae s.s.). Bot Rev 74:132–165
doi: 10.1007/s12229-008-9003-y
van Ee BW, Riina R, Berry PE (2011) A revised infrageneric classification and molecular phylogeny of new world Croton (Euphorbiaceae). Taxon 60:791–823. https://doi.org/10.1002/tax.603013
doi: 10.1002/tax.603013
Vanvinckenroye P, Cresens E, Decraene L-PR, Smets E (1993) A comparative floral developmental study in Pisonia, Bougainvillea and Mirabilis (Nyctaginaceae) with special emphasis on the gynoecium and floral nectaries. Bull Du Jard Botanique Natl De Belgique/bull Van De Natil Plantentuin Van België 62:69. https://doi.org/10.2307/3668267
doi: 10.2307/3668267
Venkata-Rao C, Ramalakshmi T (1968) Floral anatomy of the Euphorbiaceae–I. Some non-cyathium taxa. J Indian Bot Soc 47:278–300
Vitarelli NC, Riina R, Caruzo MBR, Fuertes-Aguilar J, Cordeiro I, Meira RMSA (2015) Foliar secretory structures in Crotoneae (Euphorbiaceae): diversity, anatomy, and evolutionary significance. Am J Bot 102:833–847
doi: 10.3732/ajb.1500017
pubmed: 26101410
Volgin SA (1988) Vergleichende Morphologie und Gefäßbündelanatomie der Blüte bei den Rivinoideae (Phytolaccaceae). Flora 181:325–337. https://doi.org/10.1016/S0367-2530(17)30371-7
doi: 10.1016/S0367-2530(17)30371-7
Ware S (2010) Croton monanthogynus and Crotonopsis elliptica (Euphorbiaceae) in Ozark rock outcrop communities: abundance, soil depth, and substrate tolerance. Northeast Naturalist 17:659–666. https://doi.org/10.1656/045.017.0411
doi: 10.1656/045.017.0411
Webster GL (1967) The genera of Euphorbiaceae in the Southeastern United States. J Arnold Arboretum 48:303–361
doi: 10.5962/p.67869
Webster GL (1975) Conspectus of a new classification of the Euphorbiaceae. Taxon 24:593–601. https://doi.org/10.2307/1220725
doi: 10.2307/1220725
Webster GL (1993) A provisional synopsis of the sections of the genus Croton (Euphorbiaceae). Taxon 42:793–823. https://doi.org/10.2307/1223265
doi: 10.2307/1223265
Webster GL (2014) Euphorbiaceae. In: Kubitzki K (ed) The families and genera of vascular plants Volume XI. Flowering plants. Eudicots: Malpighiales. Springer, London, pp 51–216
Wurdack KJ, Hoffmann P, Samuel R et al (2004) Molecular phylogenetic analysis of Phyllanthaceae (Phyllanthoideae pro parte, Euphorbiaceae sensu lato) using plastid RBCL DNA sequences. Am J Bot 91:1882–1900. https://doi.org/10.3732/ajb.91.11.1882
doi: 10.3732/ajb.91.11.1882
pubmed: 21652335
Wurdack KJ, Hoffmann P, Chase MW (2005) Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F DNA sequences. Am J Bot 92:1397–1420
doi: 10.3732/ajb.92.8.1397
pubmed: 21646159
Xu W-H, Liu W-Y, Liang Q (2018) Chemical constituents from Croton species and their biological activities. Molecules 23:2333. https://doi.org/10.3390/molecules23092333
doi: 10.3390/molecules23092333
pubmed: 30213129
pmcid: 6225158