A cytosystematic study of the Dianthus virgineus complex (Caryophyllaceae) in the Central Mediterranean

Abstract

European wild carnations (Dianthus) are represented by a high number of taxa organized in unresolved taxonomies. In particular, taxa belonging to the Dianthus virgineus L. complex in the Central Mediterranean have been delimited mainly with qualitative morphological data and still await quantitative investigations, which are vital to understand boundaries and relations among plant diversity groups. Here, we examine the phenotypic features of nuclear genome organization testing for species boundaries in this complex. We have studied the chromosome number, the total haploid length (THL), and the relative genome size (RGS) in 122 populations belonging to 25 out of 33 taxa of the complex. All the studied populations have 2n = 2x = 30 chromosomes, and the THL ranges from 14.09 to 20.71 μm. Genome size estimations support the absence of polyploidization events, but show a certain degree of variation (0.318–0.423 arbitrary units). The RGS variation is not in agreement with current taxonomic treatment, but rather shows a geographical pattern, with higher values in Sicily and Sardinia. No correlation between the THL and the RGS was detected, possibly due to the stable chromosome number and the small size of chromosomes. A number of evolutionary unique groups lower than the number of currently accepted taxa may be hypothesized.

Keywords

cytogenetics / genome size / karyosystematics / Mediterranean / plant evolution / taxonomy

References

[1] Agulló-AntónMÁ,OlmosE,Pérez-Pérez JM,AcostaM. 2013. Evaluation of ploidy level and endoreduplication in carnation (Dianthus spp.). Plant Science 201-202: 1-11.

[2] AltayD,Eroğlu HE,HamzaoğluE,KoçM. 2017. Karyotype analysis of some taxa of Dianthus section Verruculosi (Caryophyllaceae, Sileneae). Turkish Journal of Botany 41: 367-374.

[3] AltınorduF,Peruzzi L,YuY,HeX. 2016. A tool for the analysis of chromosomes: KaryoType. Taxon 65: 586-592.

[4] AstutiG,Roma-Marzio F,PeruzziL. 2017. Traditional cytotaxonomic studies: Can they still provide a solid basis in plant systematics? Flora Mediterranea 27: 91-98.

[5] BacchettaG,BrulloS. 2000. Dianthus mossanus (Caryophyllaceae), a new species from Sardinia. Portugaliae Acta Biologica 19: 295-301.

[6] BacchettaG,BrulloS, CastiM,Giusso del GaldoGP. 2010. Taxonomic revision of the Dianthus sylvestris group (Caryophyllaceae) in Central-Southern Italy, Sicily and Sardinia. Nordic Journal of Botany 28: 137-173.

[7] BrulloS,BrulloC, ColomboP,Giusso del GaldoG,IlardiV, PerroneR. 2015. Dianthus borbonicus (Caryophyllaceae), a new species from Sicily. Phytotaxa 233: 49-60.

[8] BaezaCM,FinotV, RuizE,Carrasco P,NovoaP,RosasM,Toro-Núñez O. 2018. Cytotaxonomic study of the Chilean endemic complex Alstroemeria magnifica Herb. (Alstroemeriaceae). Genetics and Molecular Biology 41: 434-441.

[9] BalaoF,Casimiro-Soriguer R,TalaveraM,HerreraJ,Talavera S. 2009. Distribution and diversity of cytotypes in Dianthus broteri as evidenced by genome size variations. Annals of Botany 104: 965-973.

[10] BalaoF,HerreraJ, TalaveraS. 2011. Phenotypic consequences of polyploidy and genome size at the microevolutionary scale: A multivariate morphological approach. New Phytologist 192: 256-265.

[11] BalaoF,ValenteLM, VargasP,Herrera J,TalaveraS. 2010. Radiative evolution of polyploid races of the Iberian carnation Dianthus broteri (Caryophyllaceae). New Phytologist 187: 542-551.

[12] BarowM,MeisterA. 2002. Lack of correlation between AT frequency and genome size in higher plants and the effect of nonrandomness of base sequences on dye binding. Cytometry 47: 1-7.

[13] BartolucciF,PeruzziL, GalassoG,Albano A,AlessandriniA,ArdenghiNMG,AstutiG, BacchettaG,Ballelli S,BanfiE,BarberisG,Bernardo L,BouvetD,BovioM,CecchiL, Di PietroR,Domina G,FascettiS,FenuG,FestiF, FoggiB,Gallo L,GottschlichG,GubelliniL,Iamonico D,IberiteM,Jiménez-MejíasP,LattanziE,Marchetti D,MartinettoE,MasinRR,MedagliP, PassalacquaNG,PecceniniS,PennesiR, PieriniB,Poldini L,ProsserF,RaimondoFM,Roma-Marzio F,RosatiL,SantangeloA,Scoppola A,ScortegagnaS,SelvaggiA,SelviF, SoldanoA,Stinca A,WagensommerRP,WilhalmT,ContiF. 2018. An updated checklist of the vascular flora native to Italy. Plant Biosystems 152: 179-303.

[14] BediniG,PeruzziL. 2021. Chrobase.it-Chromosome numbers for the Italian flora v. 2.0 [online]. Available from https://bot.biologia.unipi.it/chrobase/[accessed 27 January 2023].

[15] BehroozianM,VaeziJ, JoharchiMR. 2012. A karyological study of some Dianthus L. species (Caryophyllaceae) in Northeast of Iran. Feddes Repertorium 123: 265-272.

[16] BernalM,Laínz M,Muñoz GarmendiaF. 1990. Dianthus L. In: Bolibar SC ed. Flora Iberica. Madrid: Real Jardín Botánico, C.S.I.C. 2: 426-462.

[17] BrulloS,GuarinoR. 2017. Complesso di Dianthus sylvestris. In: Pignatti S ed. Flora d’Italia. Milan: New Business Media. 2: 200-205.

[18] BrulloS,GuarinoR. 2019. Complesso di Dianthus sylvestris. In: Pignatti S ed. Flora d’Italia. Milan: New Business Media. 4: 77-81.

[19] CakovićD,CrestiL, SteševićD,SchönswetterP,Frajman B. 2021. High genetic and morphological diversification of the Euphorbia verrucosa alliance (Euphorbiaceae) in the Balkan and Iberian peninsulas. Taxon 70: 286-307.

[20] CarolinRC. 1957. Cytological and hybridization studies in the genus Dianthus. New Phytologist 56: 81-97.

[21] CartaA,Fernández-Pascual E,GioriaM,MüllerJV,Rivière S,RosbakhS,SaatkampA,Vandelook F,MattanaE. 2022a. Climate shapes the seed germination niche of temperate flowering plants: A meta-analysis of European seed conservation data. Annals of Botany 129: 775-786.

[22] CartaA,MattanaE, DickieJ,Vandelook F. 2022b. Correlated evolution of seed mass and genome size varies among life forms in flowering plants. Seed Science Research 32: 46-52.

[23] CartaA,PeruzziL. 2016. Testing the large genome constraint hypothesis: Plant traits, habitat and climate seasonality in Liliaceae. New Phytologist 210: 709-716.

[24] CastroI,RochaJ, MartinsM,Carnide V,MartínJP,VeigaP,SerafimAB, AmichF,Ramírez-Rodríguez R,ColomboG,CrespíAL. 2022. The redundancy effect under morphogenetic and environmental fluctuations. The case of the Dianthus pungens group. Plant Biosystems 156: 292-306.

[25] CohenJ. 1988. Statistical power analysis for the behavioral sciences. Hillsdale: L. Erlbaum Associates.

[26] CrestiL,Schönswetter P,PeruzziL,BarfussMHJ,FrajmanB. 2019. Pleistocene survival in three Mediterranean refugia: Origin and diversification of the Italian endemic Euphorbia gasparrinii from the E. verrucosa alliance (Euphorbiaceae). Botanical Journal of the Linnean Society 189: 262-280.

[27] DarlingtonCD,WylieAP. 1956. Chromosome atlas of flowering plants. London: George Allen and Unwin Ltd.

[28] De VescoviMA,SziklaiO. 1975. Comparative analysis of Douglas fir,Pseudotsuga menziesii (Mirb.) Franco. Silvae Genetica 24: 68-73.

[29] DoleželJ,Bartoš J. 2005. Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany 95: 99-110.

[30] DoleželJ,Sgorbati S,LucrettiS. 1992. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiologia Plantarum 85: 625-631.

[31] DominaG,AstutiG, BacchettaG,Barone G,RešetnikI,TerlevićA,Thiébaut M,PeruzziL. 2021a. Typification of 14 names in the Dianthus virgineus group (Caryophyllaceae). Phytokeys 187: 1-14.

[32] DominaG,AstutiG, BaroneG,Gargano D,MinutoL,VaraldoL,PeruzziL. 2021b. Lectotypification of the Linnaean name Dianthus virgineus (Caryophyllaceae) and its taxonomic consequences. Taxon 70: 1096-1100.

[33] DominaG,Scibetta S,ScafidiF,GiovinoA. 2017. Contribution to the identification of Dianthus rupicola (Caryophyllaceae) subspecies using morphological and molecular approaches. Phytotaxa 291: 17-32.

[34] Domínguez-DelgadoJJ,López-JuradoJ,Mateos-Naranjo E,BalaoF. 2021. Phenotypic diploidization in plant functional traits uncovered by synthetic neopolyploids in Dianthus broteri. Journal of Experimental Botany 72: 5522-5533.

[35] FaizullahL,MortonJA, Hersch-GreenEI,WalczykAM,LeitchAR, LeitchIJ. 2021. Exploring environmental selection on genome size in angiosperms. Trends in Plant Science 26: 1039-1049.

[36] FassouG,Korotkova N,NersesyanA,KochMA,Dimopoulos P,BorschT. 2022. Taxonomy of Dianthus (Caryophyllaceae)-Overall phylogenetic relationships and assessment of species diversity based on a first comprehensive checklist of the genus. Phytokeys 196: 91-214.

[37] FrajmanB,Záveská E,GamischA,MoserT,Schönswetter P. 2019. Integrating phylogenomics, phylogenetics, morphometrics, relative genome size and ecological niche modelling disentangles the diversification of Eurasian Euphorbia seguieriana s.l. (Euphorbiaceae). Molecular Phylogenetics and Evolution 134: 238-252.

[38] FrajmanB,Rešetnik I,Weiss-SchneeweissH, EhrendorferF,SchönswetterP. 2015. Cytotype diversity and genome size variation in Knautia (Caprifoliaceae, Dipsacoideae). BMC Evolutionary Biology 15: 140.

[39] FrajmanB,Schönswetter P,Weiss-SchneeweissH, OxelmanB. 2018. Origin and diversification of South American polyploid Silene sect. Physolychnis (Caryophyllaceae) in the Andes and Patagonia. Frontiers in Genetics 9: 639.

[40] GamesPA,HowellJF. 1976. Pairwise multiple comparison procedures with unequal N’s and/or variances: A Monte Carlo study. Journal of Educational Statistics 1: 113.

[41] GarganoD,Franzoni J,LuqmanH,FiorS,RovitoS, PeruzziL. 2023. Phenotypic correlates of genetic divergence suggest at least three species in the complex of Dianthus virgineus L. (Caryophyllaceae). Taxon.

[42] GiacòA,De Giorgi P,AstutiG,VaraldoL,Sáez L,CarballalR,SerranoM,CasazzaG, CaputoP,Bacchetta G,PeruzziL. 2022. Diploids and polyploids in the Santolina chamaecyparissus complex (Asteraceae) show different karyotype asymmetry. Plant Biosystems 156: 1237-1246.

[43] GoulaK,Touloumis K,DimopoulosP,ConstantinidisT. 2022. A morphometric and karyological study of the Anthemis macedonica group (Asteraceae, Anthemideae) reveals a new species from Greece. Plants 11: 3006.

[44] GuerraM. 2012. Cytotaxonomy: The end of childhood. Plant Biosystems 146: 703-710.

[45] HardionL,PerrierA, MartinezM,Navrot N,GaquerelE,TournayF,Nguefack J,CombrouxI. 2020. Integrative revision of Dianthus superbus subspecies reveals different degrees of differentiation, from plasticity to species distinction. Systematics and Biodiversity 18: 255-268.

[46] HlouškováP,MandákováT,PouchM,Trávníček P,LysakMA. 2019. The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Annals of Botany 124: 103-120.

[47] JafariA,Behroozian M. 2010. A cytotaxonomic study on Dianthus L. species in North Eastern Iran. Asian Journal of Plant Sciences 9: 58-62.

[48] JanišováM,SkokanováK,Hlásny T. 2018. Ecological differentiation, speciation, and rarity: How do they match in Tephroseris longifolia agg. (Asteraceae)? Ecology and Evolution 8: 2453-2470.

[49] JoubèsJ,Chevalier C. 2000. Endoreduplication in higher plants. Plant Molecular Biology 43: 735-745.

[50] KangM,TaoJ, WangJ,Ren C,QiQ,XiangQ,HuangH. 2014. Adaptive and nonadaptive genome size evolution in Karst endemic flora of China. New Phytologist 202: 1371-1381.

[51] KassambaraA 2021. rstatix: Pipe-friendly framework for basic statistical tests. R package version 0.7.0 [online]. Available from https://CRAN.R-project.org/package=rstatix [accessed 20 December 2022].

[52] KnightCA. 2005. The large genome constraint hypothesis: Evolution, ecology and phenotype. Annals of Botany 95: 177-190.

[53] KolářF,Štech M,Trávníček P,RauchováJ,UrfusT,Vít P,KubešováM, SudaJ. 2009. Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: Primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Annals of Botany 103: 963-974.

[54] KolářF,Lučanová M,VítP,UrfusT,ChrtekJ, FérT,Ehrendorfer F,SudaJ. 2013. Diversity and endemism in deglaciated areas: Ploidy, relative genome size and niche differentiation in the Galium pusillum complex (Rubiaceae) in Northern and Central Europe. Annals of Botany 111: 1095-1108.

[55] KraaijeveldK. 2010. Genome size and species diversification. Evolutionary Biology 37: 227-233.

[56] KramerEM,Tayjasanant PA,CordoneB. 2021. Scaling laws for mitotic chromosomes. Frontiers in Cell and Developmental Biology 9: 684278.

[57] KutnjakD,KuttnerM, NiketićM,DullingerS,Schönswetter P,FrajmanB. 2014. Escaping to the summits: Phylogeography and predicted range dynamics of Cerastium dinaricum, an endangered high mountain plant endemic to the western Balkan Peninsula. Molecular Phylogenetics and Evolution 78: 365-374.

[58] LazarevićM,Kuzmanović N,LakušićD, AlegroA,Schönswetter P,FrajmanB. 2015. Patterns of cytotype distribution and genome size variation in the genus Sesleria Scop. (Poaceae). Botanical Journal of the Linnean Society 179: 126-143.

[59] LevinDA. 2002. The role of chromosomal change in plant evolution. Oxford &New York: Oxford University Press.

[60] LiuL,AstutiG, CoppiA,Peruzzi L. 2022. Different chromosome numbers but slight morphological differentiation and genetic admixture among populations of the Pulmonaria hirta complex (Boraginaceae). Taxon 75: 1025-1043.

[61] López-JuradoJ,Mateos-Naranjo E,BalaoF. 2019. Niche divergence and limits to expansion in the high polyploid Dianthus broteri complex. New Phytologist 222: 1076-1087.

[62] LoureiroJ,Trávníček P,RauchováJ,UrfusT,Vít P,ŠtechM,CastroS,SudaJ. 2010. The use of flow cytometry in the biosystematics, ecology and population biology of homoploid plants. Preslia 82: 3-21.

[63] Löve Á ed. 1968. IOPB chromosome number reports: XVIII. Taxon 17: 419-422.

[64] LuqmanH,WegmannD, FiorS,Widmer A. 2023. Climate-induced range shifts drive adaptive response via spatio-temporal sorting of alleles. Nature Communications 14: 1080.

[65] MacasJ,Novák P,PellicerJ,ČížkováJ,KoblížkováA,NeumannP,Fuková I,DoleželJ,KellyLJ,LeitchIJ. 2015. In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS One 10: e0143424.

[66] MarholdK. 2011. Caryophyllaceae. The Euro+Med Plantbase Project [online]. Available from https://ww2.bgbm.org/EuroPlusMed/PTaxonDetail.asp?NameCache=Dianthus&PTRefFk=7200000 [accessed 27 January 2023].

[67] MehraviS,Karimzadeh G,KordenaeejA,HanifeiM. 2022. Mixed-ploidy and dysploidy in Hypericum perforatum: A karyomorphological and genome size study. Plants 11: 3068.

[68] MeyerFK. 2011. Beiträge zur Flora von Albanien. Oberhof: Thüringische Botanische Gesellschaft eV.

[69] MirandaM,AlmeidaCCS, GuerraM. 2007. Karyotype of Araucaria angustifolia and the decondensation/activation mode of its nucleolus organiser region. Australian Journal of Botany 55: 165-170.

[70] Nieto FelinerG. 2014. Patterns and processes in plant phylogeography in the Mediterranean Basin. A review. Perspectives in Plant Ecology, Evolution and Systematics 16: 265-278.

[71] NiketićM,Siljak-Yakovlev S,FrajmanB,LazarevićM,Stevanović B,TomovićG,StevanovićV. 2013. Towards resolving the systematics of Cerastium subsection Cerastium (Caryophyllaceae): A cytogenetic approach. Botanical Journal of the Linnean Society 172: 205-224.

[72] PellicerJ,HidalgoO, DodsworthS,Leitch I. 2018. Genome size diversity and its impact on the evolution of land plants. Genes 9: 88.

[73] PeruzziL,Altınordu F. 2014. A proposal for a multivariate quantitative approach to infer karyological relationships among taxa. Comparative Cytogenetics 8: 337-349.

[74] PeruzziL,LeitchIJ, CaparelliKF. 2009. Chromosome diversity and evolution in Liliaceae. Annals of Botany 103: 459-475.

[75] PoggioL,RealiniMF, FourastiéMF,GarcíaAM,González GE. 2014. Genome downsizing and karyotype constancy in diploid and polyploid congeners: A model of genome size variation. AoB Plants 6: plu029.

[76] R CoreTeam. 2020. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available from https://www.R-project.org/[accessed 20 December 2022].

[77] RaimondoFM,DominaG, SpadaroV. 2010. Checklist of the vascular flora of Sicily. Quaderni di Botanica Ambientale e Applicata 21: 189-252.

[78] RaimondoFM,Rossitto M,OttonelloD. 1983. Numeri cromosomici per la flora italiana:983-992. Informatore Botanico Italiano 15(2-3): 180-187.

[79] RiceA,GlickL, AbadiS,Einhorn M,KopelmanNM,Salman-MinkovA,MayzelJ, ChayO,Mayrose I. 2015. The Chromosome Counts Database (CCDB)-A community resource of plant chromosome numbers. New Phytologist 206: 19-26.

[80] ŞahinE,Eroğlu HE,HamzaoğluE,KoçM. 2016. Karyotype analysis of four species of Dianthus section Fimbriati (Caryophyllaceae, Sileneae). Caryologia 69: 267-272.

[81] SchleyRJ,Pellicer J,GeX,BarrettC,BellotS, GuignardMS,Novák P,SudaJ,FraserD,BakerWJ, DodsworthS,Macas J,LeitchAR,LeitchIJ. 2022. The ecology of palm genomes: Repeat-associated genome size expansion is constrained by aridity. New Phytologist 236: 433-446.

[82] SchönswetterP,Suda J,PoppM,Weiss-SchneeweissH,Brochmann C. 2007. Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Molecular Phylogenetics and Evolution 42: 92-103.

[83] ŠmardaP,Bureš P. 2006. Intraspecific DNA content variability in Festuca pallens on different geographical scales and ploidy levels. Annals of Botany 98: 665-678.

[84] SudaJ,Krahulcová A,Trávníček P,RosenbaumováR, PeckertT,Krahulec F. 2007a. Genome size variation and species relationships in Hieracium sub-genus Pilosella (Asteraceae) as inferred by flow cytometry. Annals of Botany 100: 1323-1335.

[85] SudaJ,KronP, HusbandBC,Trávníček P. 2007b. Flow cytometry and ploidy: Applications in plant systematics, ecology and evolutionary biology. In: Doležel J,Greilhuber J,Suda J eds. Flow cytometry with plant cells. Hoboken: John Wiley & Sons Ltd. 103-130.

[86] SudaJ,Trávníček P. 2006. Estimation of relative nuclear DNA content in dehydrated plant tissues by flow cytometry. Current Protocols in Cytometry 38: 7-30.

[87] TerlevićA,Bogdanović S,FrajmanB,RešetnikI. 2022. Genome size variation in Dianthus sylvestris Wulfen sensu lato (Caryophyllaceae). Plants 11: 1481.

[88] TerlevićA,Temunović M,BogdanovićS, GrgurevM,Ljubičić I,RešetnikI. 2023. Morphological and environmental variability of Dianthus sylvestris (Caryophyllaceae) in the Balkan Peninsula. Botanical Journal of the Linnean Society 201: 377-389.

[89] ThompsonJD. 2020. Plant evolution in the Mediterranean: Insights for conservation. New York: Oxford University Press Inc.

[90] TiburtiniM,AstutiG, BartolucciF,Casazza G,VaraldoL,De LucaD,Bottigliero MV,BacchettaG,PorcedduM,DominaG, OrsenigoS,Peruzzi L. 2022. Integrative taxonomy of Armeria arenaria (Plumbaginaceae), with a special focus on the putative subspecies endemic to the Apennines. Biology 11: 1060.

[91] TisonJ-M,de Foucault B. 2014. Flora Gallica: Flore de France. Mèze: Biotope Éditions.

[92] TisonJ-M,JauzeinP, MichaudH. 2014. Flore de la France méditerranéenne continentale. Turriers: Naturalia Publications.

[93] TrávníčekP,ČertnerM,PonertJ, ChumováZ,JersákováJ,SudaJ. 2019. Diversity in genome size and GC content shows adaptive potential in orchids and is closely linked to partial endoreplication, plant life-history traits and climatic conditions. New Phytologist 224: 1642-1656.

[94] TutinTG. 1993. Dianthus L. In: Tutin TG,Burges NA,Chater AD,Edmondson JR,Heywood VH,Moore DM,Valentine DH,Walters SM,Webb DA eds. Flora Europaea. Cambridge: Cambridge University Press. 1: 227-246.

[95] TurcoA,AlbanoA, MedagliP,Pulvirenti S,D’EmericoS. 2018. New cytological data in Ophrys sect. Pseudophrys Godfery and comparative karyomorphological studies in Ophrys L. (Orchidaceae). Plant Biosystems 152: 901-919.

[96] ValenteLM,Savolainen V,VargasP. 2010. Unparalleled rates of species diversification in Europe. Proceedings of the Royal Society B: Biological Sciences 277: 1489-1496.

[97] WeissH,Dobeš C,SchneeweissG,GreimlerJ. 2002. Occurrence of tetraploid and hexaploid cytotypes between and within populations in Dianthus sect Plumaria (Caryophyllaceae). New Phytologist 156: 85-94.

[98] WinterfeldG,LeyA, HoffmannMH,Paule J,RöserM. 2020. Dysploidy and polyploidy trigger strong variation of chromosome numbers in the prayer-plant family (Marantaceae). Plant Systematics and Evolution 306: 36.

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