Morphological and Genomic Differences in the Italian Populations of Onopordum tauricum Willd.—A New Source of Vegetable Rennet
Abstract
:1. Introduction
2. Results
2.1. Genetic Structure Analysis
2.2. Phylogenetic Tree
2.3. Morphometric Characterization
3. Discussion
4. Materials and Methods
4.1. Species Identification
4.2. Plant Collection and DNA Isolation
4.3. RADseq Library Preparation and Sequencing
4.4. Identification of RAD Loci and SNP Calling
4.5. Phylogenetic Analysis
4.6. Morphometric Analysis
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Jacob, M.; Jaros, D.; Rohm, H. Recent Advances in Milk Clotting Enzymes. Int. J. Dairy Tech. 2011, 64, 14–33. [Google Scholar] [CrossRef]
- Roseiro, L.B.; Barbosa, M.; Ames, J.M.; Wilbey, R.A. Cheesemaking with Vegetable Coagulants—The Use of Cynara L. for the Production of Ovine Milk Cheeses. Int. J. Dairy Tech. 2003, 56, 76–85. [Google Scholar] [CrossRef]
- Nicosia, F.D.; Puglisi, I.; Pino, A.; Caggia, C.; Randazzo, C.L. Plant Milk-Clotting Enzymes for Cheesemaking. Foods 2022, 11, 871. [Google Scholar] [CrossRef] [PubMed]
- Mozzon, M.; Foligni, R.; Mannozzi, C.; Zamporlini, F.; Raffaelli, N.; Aquilanti, L. Clotting Properties of Onopordum tauricum (Willd.) Aqueous Extract in Milk of Different Species. Foods 2020, 9, 692. [Google Scholar] [CrossRef] [PubMed]
- Foligni, R.; Mannozzi, C.; Gasparrini, M.; Raffaelli, N.; Zamporlini, F.; Tejada, L.; Bande-De León, C.; Orsini, R.; Manzi, P.; Di Costanzo, M.G.; et al. Potentialities of Aqueous Extract from Cultivated Onopordum tauricum (Willd.) as Milk Clotting Agent for Cheesemaking. Food Res. Int. 2022, 158, 111592. [Google Scholar] [CrossRef]
- Rampanti, G.; Belleggia, L.; Cardinali, F.; Milanović, V.; Osimani, A.; Garofalo, C.; Ferrocino, I.; Aquilanti, L. Microbial Dynamics of a Specialty Italian Raw Ewe’s Milk Cheese Curdled with Extracts from Spontaneous and Cultivated Onopordum tauricum Willd. Microorganisms 2023, 11, 219. [Google Scholar] [CrossRef] [PubMed]
- Zenobi, S.; Fiorentini, M.; Aquilanti, L.; Foligni, R.; Mannozzi, C.; Mozzon, M.; Zitti, S.; Casavecchia, S.; Al Mohandes Dridi, B.; Orsini, R. Effect of Planting Density in Two Thistle Species Used for Vegetable Rennet Production in Marginal Mediterranean Areas. Agronomy 2021, 11, 135. [Google Scholar] [CrossRef]
- Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available online: http://www.plantsoftheworldonline.org/ (accessed on 15 January 2024).
- Groves, R.H.; Moerkerk, M.; Blakey, D.; Moore, P.H.R. Taurian Thistle in Australia—A Candidate for Eradication? In Proceedings of the 13th Australian Weeds Conference: Weeds “Threats Now and Forever?”, Perth, WA, Australia, 8–13 September 2002; Plant Protection Society of Western Australia Inc.: Victoria Park, WA, Australia, 2002; pp. 287–288. [Google Scholar]
- Briese, D.T.; Pettit, W.J.; Swirepik, A.; Walker, A. A Strategy for the Biological Control of Onopordum Spp. Thistles in South-Eastern Australia. Biocontrol Sci. Technol. 2002, 12, 121–136. [Google Scholar] [CrossRef]
- Häffner, E.; Hellwig, F.H. Phylogeny of the Tribe Cardueae (Compositae) with Emphasis on the Subtribe Carduinae: An Analysis Based on ITS Sequence Data. Willdenowia 1999, 29, 27. [Google Scholar] [CrossRef]
- Garcia-Jacas, N.; Garnatje, T.; Susanna, A.; Vilatersana, R. Tribal and Subtribal Delimitation and Phylogeny of the Cardueae (Asteraceae): A Combined Nuclear and Chloroplast DNA Analysis. Mol. Phylogenetics Evol. 2002, 22, 51–64. [Google Scholar] [CrossRef]
- Susanna, A.; Garcia-Jacas, N.; Hidalgo, O.; Vilatersana, R.; Garnatje, T. The Carduae (Compositae) Revisited: Insights from ITS, trnL-trnF, and matK Nuclear and Chloroplast DNA Analysis. Ann. Mo. Bot. Gard. 2006, 93, 150–171. [Google Scholar] [CrossRef]
- Susanna, A.; Garcia-Jacas, N. Tribe Cardueae Cass. (1819). In Flowering Plants, Eudicots Asterales, the Families and Genera of Vascular Plants; Springer: Berlin/Heidelberg, Germany, 2007; Volume 8, pp. 123–146. [Google Scholar]
- Barres, L.; Sanmartín, I.; Anderson, C.L.; Susanna, A.; Buerki, S.; Galbany-Casals, M.; Vilatersana, R. Reconstructing the Evolution and Biogeographic History of Tribe Cardueae (Compositae). Am. J. Bot. 2013, 100, 867–882. [Google Scholar] [CrossRef] [PubMed]
- Herrando-Moraira, S.; Calleja, J.A.; Galbany-Casals, M.; Garcia-Jacas, N.; Liu, J.-Q.; López-Alvarado, J.; López-Pujol, J.; Mandel, J.R.; Massó, S.; Montes-Moreno, N.; et al. Nuclear and Plastid DNA Phylogeny of Tribe Cardueae (Compositae) with Hyb-Seq Data: A New Subtribal Classification and a Temporal Diversification Framework. Mol. Phylogenetics Evol. 2019, 137, 313–332. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Jacas, N.; Galbany-Casals, M.; Romashchenko, K.; Susanna, A. On the Conflicting Generic Delineation in the Onopordum Group (Compositae, Cardueae—Carduinae): A Combined Nuclear and Plastid Molecular Approach. Aust. Syst. Bot. 2008, 21, 301. [Google Scholar] [CrossRef]
- Susanna, A.; Garcia-Jacas, N. Cardueae (Carduoideae). In Systematics, Evolution, and Biogeography of Compositae; IAPT: Vienna, Austria, 2009; pp. 293–314. [Google Scholar]
- Zhang, C.; Huang, C.; Liu, M.; Hu, Y.; Panero, J.L.; Luebert, F.; Gao, T.; Ma, H. Phylotranscriptomic Insights into Asteraceae Diversity, Polyploidy, and Morphological Innovation. J. Integr. Plant Biol. 2021, 63, 1273–1293. [Google Scholar] [CrossRef]
- Acta Plantaurum. Available online: https://www.actaplantarum.org/ (accessed on 15 January 2024).
- Euro+Med PlantBase. Available online: https://europlusmed.org/ (accessed on 15 January 2024).
- Pignatti, S. Flora d’Italia. 3, 1st ed.; Edagricole: Bologna, Italy, 1982; ISBN 978-88-206-2312-8. [Google Scholar]
- Pignatti, S. Flora d’Italia. Volume 3; Seconda edizione in 4 volumi; Edagricole: Milano, Italy, 2018; ISBN 978-88-506-5244-0. [Google Scholar]
- World Flora Online. Available online: https://www.worldfloraonline.org/ (accessed on 20 January 2024).
- Chalvin, C.; Drevensek, S.; Dron, M.; Bendahmane, A.; Boualem, A. Genetic Control of Glandular Trichome Development. Trends Plant Sci. 2020, 25, 477–487. [Google Scholar] [CrossRef] [PubMed]
- Feng, Z.; Bartholomew, E.S.; Liu, Z.; Cui, Y.; Dong, Y.; Li, S.; Wu, H.; Ren, H.; Liu, X. Glandular Trichomes: New Focus on Horticultural Crops. Hortic. Res. 2021, 8, 158. [Google Scholar] [CrossRef] [PubMed]
- Han, G.; Li, Y.; Yang, Z.; Wang, C.; Zhang, Y.; Wang, B. Molecular Mechanisms of Plant Trichome Development. Front. Plant Sci. 2022, 13, 910228. [Google Scholar] [CrossRef]
- Werker, E. Trichome Diversity and Development. In Advances in Botanical Research; Elsevier: Marseille, France, 2000; Volume 31, pp. 1–35. ISBN 978-0-12-005931-7. [Google Scholar]
- Liakoura, V.; Stavrianakou, S.; Liakopoulos, G.; Karabourniotis, G.; Manetas, Y. Effects of UV-B Radiation on Olea Europaea: Comparisons between a Greenhouse and a Field Experiment. Tree Physiol. 1999, 19, 905–908. [Google Scholar] [CrossRef]
- Klich, M.G. Leaf Variations in Elaeagnus Angustifolia Related to Environmental Heterogeneity. Environ. Exp. Bot. 2000, 44, 171–183. [Google Scholar] [CrossRef]
- Yamazaki, K.; Lev-Yadun, S. Dense White Trichome Production by Plants as Possible Mimicry of Arthropod Silk or Fungal Hyphae That Deter Herbivory. J. Theor. Biol. 2015, 364, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Janzen, D.H.; Martin, P.S. Neotropical Anachronisms: The Fruits the Gomphotheres Ate. Science 1982, 215, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Cooper, S.M.; Owen-Smith, N. Effects of Plant Spinescence on Large Mammalian Herbivores. Oecologia 1986, 68, 446–455. [Google Scholar] [CrossRef] [PubMed]
- Janzen, D.H. Chihuahuan Desert Nopaleras: Defaunated Big Mammal Vegetation. Annu. Rev. Ecol. Syst. 1986, 17, 595–636. [Google Scholar] [CrossRef]
- Myers, J.H.; Bazely, D. Thorns, Spines, Prickles, and Hairs: Are They Stimulated by Herbivory and Do They Deter Herbivores? In Phytochemical Induction by Herbivores; John Wiley and Sons: New York, NY, USA, 1991; pp. 325–344. [Google Scholar]
- Grubb, P.J. A Positive Distrust in Simplicity–Lessons from Plant Defences and from Competition among Plants and among Animals. J. Ecol. 1992, 80, 585–610. [Google Scholar] [CrossRef]
- Gowda, J.H. Spines of Acacia Tortilis: What Do They Defend and How? Oikos 1996, 77, 279. [Google Scholar] [CrossRef]
- Rebollo, S.; Milchunas, D.G.; Noy-Meir, I.; Chapman, P.L. The Role of a Spiny Plant Refuge in Structuring Grazed Shortgrass Steppe Plant Communities. Oikos 2002, 98, 53–64. [Google Scholar] [CrossRef]
- Halpern, M.; Raats, D.; Lev-Yadun, S. Plant Biological Warfare: Thorns Inject Pathogenic Bacteria into Herbivores. Environ. Microbiol. 2007, 9, 584–592. [Google Scholar] [CrossRef]
- Halpern, M.; Raats, D.; Lev-Yadun, S. The Potential Anti-Herbivory Role of Microorganisms on Plant Thorns. Plant Signal. Behav. 2007, 2, 503–504. [Google Scholar] [CrossRef]
- Lev-Yadun, S. Halpern External and Internal Spines in Plants Insert Pathogenic Microorganisms into Herbivore’s Tissues for Defense. In Microbial Ecology Research Trends; Thijs Van Dijk: New York, NY, USA, 2008; pp. 155–168. ISBN 978-1-60456-179-1. [Google Scholar]
- Belete, T. Defense Mechanisms of Plants to Insect Pests: From Morphological to Biochemical Approach. Trends Tech. Sci. Res. 2018, 2, 555584. [Google Scholar] [CrossRef]
- Kariyat, R.R.; Hardison, S.B.; De Moraes, C.M.; Mescher, M.C. Plant Spines Deter Herbivory by Restricting Caterpillar Movement. Biol. Lett. 2017, 13, 20170176. [Google Scholar] [CrossRef] [PubMed]
- Mostafa, S.; Wang, Y.; Zeng, W.; Jin, B. Plant Responses to Herbivory, Wounding, and Infection. Int. J. Mol. Sci. 2022, 23, 7031. [Google Scholar] [CrossRef] [PubMed]
- Ronel, M.; Khateeb, S.; Lev-Yadun, S. Protective Spiny Modules in Thistles of the Asteraceae in Israel. J. Torrey Bot. Soc. 2009, 136, 46–56. [Google Scholar] [CrossRef]
- Leichty, A.R.; Poethig, R.S. Development and Evolution of Age-Dependent Defenses in Ant-Acacias. Proc. Natl. Acad. Sci. USA 2019, 116, 15596–15601. [Google Scholar] [CrossRef] [PubMed]
- Tsukaya, H. Developmental Genetics of Leaf Morphogenesis in Dicotyledonous Plants. J. Plant Res. 1995, 108, 407–416. [Google Scholar] [CrossRef]
- Hofer, J.; Gourlay, C.W.; Ellis, N. Genetic Control of Leaf Morphology: A Partial View. Ann. Bot. 2001, 88, 1129–1139. [Google Scholar] [CrossRef]
- Kim, G.; Cho, K. Recent Advances in the Genetic Regulation of the Shape of Simple Leaves. Physiol. Plant. 2006, 126, 494–502. [Google Scholar] [CrossRef]
- Kimura, S.; Koenig, D.; Kang, J.; Yoong, F.Y.; Sinha, N. Natural Variation in Leaf Morphology Results from Mutation of a Novel KNOX Gene. Curr. Biol. 2008, 18, 672–677. [Google Scholar] [CrossRef]
- Baerenfaller, K.; Massonnet, C.; Walsh, S.; Baginsky, S.; Bühlmann, P.; Hennig, L.; Hirsch-Hoffmann, M.; Howell, K.A.; Kahlau, S.; Radziejwoski, A.; et al. Systems-based Analysis of Arabidopsis Leaf Growth Reveals Adaptation to Water Deficit. Mol. Syst. Biol. 2012, 8, 606. [Google Scholar] [CrossRef]
- Chitwood, D.H.; Ranjan, A.; Martinez, C.C.; Headland, L.R.; Thiem, T.; Kumar, R.; Covington, M.F.; Hatcher, T.; Naylor, D.T.; Zimmerman, S.; et al. A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape. Plant Physiol. 2014, 164, 259–272. [Google Scholar] [CrossRef]
- Yang, W.; Guo, Z.; Huang, C.; Wang, K.; Jiang, N.; Feng, H.; Chen, G.; Liu, Q.; Xiong, L. Genome-Wide Association Study of Rice (Oryza sativa L.) Leaf Traits with a High-Throughput Leaf Scorer. J. Exp. Bot. 2015, 66, 5605–5615. [Google Scholar] [CrossRef] [PubMed]
- Xu, P.; Ali, A.; Han, B.; Wu, X. Current Advances in Molecular Basis and Mechanisms Regulating Leaf Morphology in Rice. Front. Plant Sci. 2018, 9, 1528. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Zhang, S.; Ye, M.; Jiang, L.; Vallejos, C.E.; Wu, R. The Genetic Control of Leaf Allometry in the Common Bean, Phaseolus Vulgaris. BMC Genet. 2020, 21, 29. [Google Scholar] [CrossRef]
- Quan, M.; Liu, X.; Du, Q.; Xiao, L.; Lu, W.; Fang, Y.; Li, P.; Ji, L.; Zhang, D. Genome-Wide Association Studies Reveal the Coordinated Regulatory Networks Underlying Photosynthesis and Wood Formation in Populus. J. Exp. Bot. 2021, 72, 5372–5389. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.-L.; Li, X.-G.; Xu, X.-H.; Chen, H.-P.; Li, Y.-L.; Guy, R.D. Leaf Morphology, Photosynthesis and Pigments Change with Age and Light Regime in Savin Juniper. Plant Biol. J. 2021, 23, 1097–1108. [Google Scholar] [CrossRef] [PubMed]
- Tian, F.; Bradbury, P.J.; Brown, P.J.; Hung, H.; Sun, Q.; Flint-Garcia, S.; Rocheford, T.R.; McMullen, M.D.; Holland, J.B.; Buckler, E.S. Genome-Wide Association Study of Leaf Architecture in the Maize Nested Association Mapping Population. Nat. Genet. 2011, 43, 159–162. [Google Scholar] [CrossRef] [PubMed]
- Sun, X.; Gao, Y.; Lu, Y.; Zhang, X.; Luo, S.; Li, X.; Liu, M.; Feng, D.; Gu, A.; Chen, X.; et al. Genetic Analysis of the “Head Top Shape” Quality Trait of Chinese Cabbage and Its Association with Rosette Leaf Variation. Hortic. Res. 2021, 8, 106. [Google Scholar] [CrossRef] [PubMed]
- Du, J.; Li, B.; Lu, X.; Yang, X.; Guo, X.; Zhao, C. Quantitative Phenotyping and Evaluation for Lettuce Leaves of Multiple Semantic Components. Plant Methods 2022, 18, 54. [Google Scholar] [CrossRef]
- Zhang, M.; Liu, B.; Fei, Y.; Yang, X.; Zhao, L.; Shi, C.; Zhang, Y.; Lu, N.; Wu, C.; Ma, W.; et al. Genetic Architecture of Leaf Morphology Revealed by Integrated Trait Module in Catalpa bungei. Hortic. Res. 2023, 10, uhad032. [Google Scholar] [CrossRef]
- Tsukaya, H. Leaf Shape: Genetic Controls and Environmental Factors. Int. J. Dev. Biol. 2005, 49, 547–555. [Google Scholar] [CrossRef]
- Subashri, M.; Robin, S.; Vinod, K.K.; Rajeswari, S.; Mohanasundaram, K.; Raveendran, T.S. Trait Identification and QTL Validation for Reproductive Stage Drought Resistance in Rice Using Selective Genotyping of near Flowering RILs. Euphytica 2009, 166, 291–305. [Google Scholar] [CrossRef]
- Li, Y.-H.; Lu, Q.; Wu, B.; Zhu, Y.-J.; Liu, D.-J.; Zhang, J.-X.; Jin, Z.-H. A Review of Leaf Morphology Plasticity Linked to Plant Response and Adaptation Characteristics in Arid Ecosystems. Chin. J. Plant Ecol. 2012, 36, 88–98. [Google Scholar] [CrossRef]
- Fu, G.; Dai, X.; Symanzik, J.; Bushman, S. Quantitative Gene–Gene and Gene–Environment Mapping for Leaf Shape Variation Using Tree-based Models. New Phytol. 2017, 213, 455–469. [Google Scholar] [CrossRef]
- Park, J.; Lee, Y.; Martinoia, E.; Geisler, M. Plant Hormone Transporters: What We Know and What We Would like to Know. BMC Biol. 2017, 15, 93. [Google Scholar] [CrossRef] [PubMed]
- Fritz, M.A.; Rosa, S.; Sicard, A. Mechanisms Underlying the Environmentally Induced Plasticity of Leaf Morphology. Front. Genet. 2018, 9, 478. [Google Scholar] [CrossRef]
- Chehregani, A.; Mahanfar, N. Achene Micro-Morphology of Anthemis (Asteraceae) and Its Allies in Iran with Emphasis on Systematics. Int. J. Agri. Biol. 2007, 9, 486–488. [Google Scholar]
- Hacioglu, B.T.; Arslan, Y.; Subasi, I.; Katar, D.; Bulbul, A.S.; Ceter, T. Achene Morphology of Turkish “Carthamus” Species. Aust. J. Crop Sci. 2012, 6, 1260–1264. [Google Scholar]
- Gabr, D.G.I. Comparative Morphological Studies on Achene of Some Taxa of Asteraceae. Arab. Univ. J. Agric. Sci. 2015, 23, 601–614. [Google Scholar] [CrossRef]
- Ghimire, B.; Jeong, M.J.; Lee, K.M.; Heo, K.; Lee, C.H.; Suh, G.U. Achene Morphology of Saussurea Species (Asteraceae, Cardueae) in Korea and Its Systematic Implications. Bot. J. Linn. Soc. 2016, 181, 692–710. [Google Scholar] [CrossRef]
- ŞiRiN, E.; Ertuğrul, K.; Uysal, T. Achene Micromorphology of the Genus Cyanus Mill. (Compositae) in Turkey and Its Taxonomic Importance. Phytotaxa 2017, 313, 77. [Google Scholar] [CrossRef]
- Skilbeck, C.A.; Lynch, I.; Ellenby, M.; Spencer, M.A. Achene Morphology of British and Irish Mayweeds and Chamomiles: Implications for Taxonomy and Identification. Br. Ir. Bot. 2019, 1, 128–166. [Google Scholar] [CrossRef]
- Adwan, A.; Al-Mashhadani, A.N.; Abas, R. Taxonomical Features of Achene of Some Species of Centaurea L.(Asteraceae) in Middle and North Iraq. EurAsian J. BioSciences 2020, 14, 5109–5114. [Google Scholar]
- Bona, M. Systematic Importance of Achene Macro-micromorphological Characteristics in Selected Species of the Genera Crupina, Jurinea, and Klasea (Asteraceae) from Turkey. Microsc. Res. Tech. 2020, 83, 1345–1353. [Google Scholar] [CrossRef]
- Shamso, E.; Hosni, H.; Ahmed, D.; Shaltout, K. Achene Characteristics of Some Taxa of Asteraceae from the Northwestern Mediterranean Coast of Egypt. Egypt. J. Bot. 2021, 61, 1–31. [Google Scholar] [CrossRef]
- Celik, S.; Uysal, I.; Menemen, Y. Centaurea Species in Turkey (A): Centaurea odyssei Wagenitz (Asteraceae) in Kazdagi (Mt. Ida) National Park. Int. J. Biodivers. Sci. Manag. 2005, 1, 113–120. [Google Scholar] [CrossRef]
- Uysal, I.; Celik, S.; Menemen, Y. Morphology, Anatomy, Ecology, Pollen and Achene Features of Centaurea Polyclada DC.(Sect. Acrolophus) in Turkey. J. Biol. Sci. 2005, 5, 176–180. [Google Scholar]
- Aksoy, N.; Ataslar, E.; Efe, A.; Güneş, N. Centaurea yaltirikii Subsp. dumanii Subsp. Nov.(C. Sect. Pseudoseridia, Asteraceae) in Marmara Region of Turkey. Int. J. Food Agric. Environ. 2010, 8, 1212–1215. [Google Scholar]
- Okay, Y.; Demir, K. Critically Endangered Endemic Centaurea Tchihatcheffii Fisch. & Mey. and Its Propagation Possibilities. Afr. J. Agric. Res. 2010, 5, 3536–3541. [Google Scholar]
- Shabestari, E.S.B.; Attar, F.; Riahi, H.; Sheidai, M. Seed Morphology of the Centaurea Species (Asteraceae) in Iran. Phytol. Balc. 2013, 19, 209–214. [Google Scholar]
- Bona, M. Achene Characteristics of Turkish Centaurea (Asteraceae) and Their Systematic Application. Bangladesh J. Bot. 2014, 43, 163–168. [Google Scholar] [CrossRef]
- Negaresh, K.; Rahiminejad, M.R. A Contribution to the Taxonomy of Centaurea Sect. Cynaroides (Asteraceae, Cardueae–Centaureinae) in Iran. Phytotaxa 2014, 158, 229. [Google Scholar] [CrossRef]
- Ranjbar, M.; Negaresh, K. A Revision of Centaurea Sect. Centaurea (Asteraceae) from Iran. Turk. J. Bot. 2014, 38, 969–987. [Google Scholar] [CrossRef]
- Bona, M. Systematic Implications of Achene Characteristics in Genera Centaurea L., Cyanus Mill., Psephellus Cass. and Rhaponticoides Vaill. (Asteraceae). Bangladesh J. Plant Taxon. 2015, 22, 125–136. [Google Scholar] [CrossRef]
- Candan, F.; Uysal, T.; Tugay, O.; Bozkurt, M.; Ertuğrul, K.; DemiRelma, H. The Examinations of Achene Ultrastructural Features of Section Acrolophus(Centaurea, Asteraceae) via Scanning Electron Microscopy. Turk. J. Bot. 2016, 40, 147–163. [Google Scholar] [CrossRef]
- Rakizadeh, S.; Attar, F.; Sotoodeh, A. Taxonomic significance of achene morphology in the genus Centaurea L. (Asteraceae). Nova Biol. Reper. 2019, 6, 352–366. [Google Scholar] [CrossRef]
- Tanksley, S.D. The Genetic, Developmental, and Molecular Bases of Fruit Size and Shape Variation in Tomato. Plant Cell Online 2004, 16, S181–S189. [Google Scholar] [CrossRef]
- Huang, Z.; Van Houten, J.; Gonzalez, G.; Xiao, H.; Van Der Knaap, E. Genome-Wide Identification, Phylogeny and Expression Analysis of SUN, OFP and YABBY Gene Family in Tomato. Mol. Genet. Genom. 2013, 288, 111–129. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Huang, D.; Tang, W.; Zheng, Y.; Liang, K.; Cutler, A.J.; Wu, W. Mapping of Quantitative Trait Loci Underlying Cold Tolerance in Rice Seedlings via High-Throughput Sequencing of Pooled Extremes. PLoS ONE 2013, 8, e68433. [Google Scholar] [CrossRef] [PubMed]
- Takagi, H.; Abe, A.; Yoshida, K.; Kosugi, S.; Natsume, S.; Mitsuoka, C.; Uemura, A.; Utsushi, H.; Tamiru, M.; Takuno, S.; et al. QTL-seq: Rapid Mapping of Quantitative Trait Loci in Rice by Whole Genome Resequencing of DNA from Two Bulked Populations. Plant J. 2013, 74, 174–183. [Google Scholar] [CrossRef] [PubMed]
- Van Der Knaap, E.; Chakrabarti, M.; Chu, Y.H.; Clevenger, J.P.; Illa-Berenguer, E.; Huang, Z.; Keyhaninejad, N.; Mu, Q.; Sun, L.; Wang, Y.; et al. What Lies beyond the Eye: The Molecular Mechanisms Regulating Tomato Fruit Weight and Shape. Front. Plant Sci. 2014, 5, 227. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.; Clevenger, J.P.; Sun, L.; Visa, S.; Kamiya, Y.; Jikumaru, Y.; Blakeslee, J.; Van Der Knaap, E. The Control of Tomato Fruit Elongation Orchestrated by Sun, Ovate and Fs8.1 in a Wild Relative of Tomato. Plant Sci. 2015, 238, 95–104. [Google Scholar] [CrossRef]
- Singh, V.K.; Khan, A.W.; Jaganathan, D.; Thudi, M.; Roorkiwal, M.; Takagi, H.; Garg, V.; Kumar, V.; Chitikineni, A.; Gaur, P.M.; et al. QTL-seq for Rapid Identification of Candidate Genes for 100-seed Weight and Root/Total Plant Dry Weight Ratio under Rainfed Conditions in Chickpea. Plant Biotechnol. J. 2016, 14, 2110–2119. [Google Scholar] [CrossRef]
- Bommisetty, R.; Chakravartty, N.; Bodanapu, R.; Naik, J.B.; Panda, S.K.; Lekkala, S.P.; Lalam, K.; Thomas, G.; Mallikarjuna, S.J.; Eswar, G.R.; et al. Discovery of Genomic Regions and Candidate Genes for Grain Weight Employing next Generation Sequencing Based QTL-Seq Approach in Rice (Oryza sativa L.). Mol. Biol. Rep. 2020, 47, 8615–8627. [Google Scholar] [CrossRef]
- Vazquez, D.V.; Pereira Da Costa, J.H.; Godoy, F.N.I.; Cambiaso, V.; Rodríguez, G.R. Genetic Basis of the Lobedness Degree in Tomato Fruit Morphology. Plant Sci. 2022, 319, 111258. [Google Scholar] [CrossRef]
- Wu, Y.; Wang, Y.; Fan, X.; Zhang, Y.; Jiang, J.; Sun, L.; Luo, Q.; Sun, F.; Liu, C. QTL Mapping for Berry Shape Based on a High-Density Genetic Map Constructed by Whole-Genome Resequencing in Grape. Hortic. Plant J. 2023, 9, 729–742. [Google Scholar] [CrossRef]
- Conti, F.; Abbate, G.; Alessandrini, A. (Eds.) An Annotated Checklist of the Italian Vascular Flora; Palombi Editori: Roma, Italy, 2005; ISBN 978-88-7621-458-5. [Google Scholar]
- Bartolucci, F.; Peruzzi, L.; Galasso, G.; Albano, A.; Alessandrini, A.; Ardenghi, N.M.G.; Astuti, G.; Bacchetta, G.; Ballelli, S.; Banfi, E.; et al. An Updated Checklist of the Vascular Flora Native to Italy. Plant Biosyst.—Int. J. Deal. All Asp. Plant Biol. 2018, 152, 179–303. [Google Scholar] [CrossRef]
- Viviani, D. Florae Libycae Specimen: Sive, Plantarum Enumeratio Cyrenaicam, Pentapolim, Magnae Syrteos Desertum et Regionem Tripolitanam Incolentium Quas ex Siccis Speciminibus Delineavit, Descripsit et Ære Insculpi Curavit; Ex Typographia Pagano: Genova, Italy, 1824. [Google Scholar]
- Rouy, M.G. Revision Du Genre Onopordon. Bull. Société Bot. Fr. 1896, 43, 577–599. [Google Scholar] [CrossRef]
- Vicioso, B.; Vicioso, C. Formas Nuevas Del Género Onopordon. Bol. Soc. Esp. Hist. Nat. 1912, 8, 457–458. [Google Scholar]
- Eig, A. Revision of the Onopordon Species of Palestine, Syria and Adjacent Countries. Palest. J. Bot. Jerus. 1942, 185–199. [Google Scholar]
- González Sierra, G.; Pérez Morales, C.; Penas Merino, A.; Rivas-Martinez, S. Revision Taxonomica de Las Especies Ibéricas Del Género onopordum L. Candollea 1992, 47, 181–213. [Google Scholar]
- Michael, P.W. Necessary Background for Studies in the Taxonomy of Onopordum in Australia. Plant Prot. Q. 1996, 11, 239–241. [Google Scholar]
- Balao, F.; Navarro-Sampedro, L.; Berjano, R.; García-Castaño, J.L.; Casimiro-Soriguer, R.; Talavera, M.; Talavera, S.; Terrab, A. Riverine Speciation and Long Dispersal Colonization in the Ibero-African Onopordum dissectum Complex (Asteraceae). Bot. J. Linn. Soc. 2017, 183, 600–615. [Google Scholar] [CrossRef]
- O’Hanlon, P.C.; Briese, D.T.; Peakall, R. Colonization of Novel Environments by Hybrid Onopordum Thistles: The Role of Habitat Variation and Founder Effects for Hybrid Zones. In Proceedings of the Third International Weed Science Congress, Foz do Iguassu, Brazil, 6 June 2000; Volume 10, pp. 3–11. [Google Scholar]
- Gordo, B.; Mostafa, N.A.M. Onopordum (Asteraceae) in Algeria with Special Focus on O. ambiguum. Fl. Medit. 2021, 31, 223–232. [Google Scholar] [CrossRef]
- Hossain, M.; Al-Sarraf, M.A.A. A New Species of Onopordum (Compositae) from Iraq. Kew Bull. 1981, 36, 159. [Google Scholar] [CrossRef]
- Townsend, C.C. A New Iraqi Species of Onopordum (Compositae): Contributions to the Flora of Iraq: XIV. Kew Bull. 1987, 42, 439. [Google Scholar] [CrossRef]
- Talavera, S.; Balao, F.; Casimiro-Soriguer, R.; Talavera Solís, M.; Terrab, A.; Ortiz Herrera, M.A. Contribuciones a La Flora Vascular de Andalucía (España). 136: Dos Especies Nuevas Del Género onopordum L. Del Litoral Atlántico (Sw de España y Nw de Marruecos). Acta Bot. Malacit. 2008, 33, 357–382. [Google Scholar] [CrossRef]
- Aytaç, Z.; Duman, H. A New Species and 2 New Records from Turkey. Turk. J. Bot. 2013, 37, 1055–1060. [Google Scholar] [CrossRef]
- Pinar, S.M.; Behçet, L. Onopordum Hasankeyfense (Asteraceae), a New Species from South-Eastern Turkey. Turk. J. Bot. 2014, 38, 226–233. [Google Scholar] [CrossRef]
- Pinar, S.M.; Eroğlu, H. Onopordum nezaketianum Sp. Nov. (Asteraceae: Cardueae): A New Species from Central Anatolia, Turkey. Turk. J. Bot. 2019, 43, 126–134. [Google Scholar] [CrossRef]
- Tutin, T.G. (Ed.) Flora Europaea. Vol. 4: Plantaginaceae to Compositae (and Rubiaceae); 1. paperback print.; Cambridge University Press: Cambridge, UK, 2010; ISBN 978-0-521-08717-9. [Google Scholar]
- Wilkie, P.; Poulsen, A.D.; Harris, D.; Forrest, L.L. The Collection and Storage of Plant Material for DNA Extraction: The Teabag Method. Gard. Bull. Singap. 2013, 65, 231–234. [Google Scholar]
- Peterson, B.K.; Weber, J.N.; Kay, E.H.; Fisher, H.S.; Hoekstra, H.E. Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species. PLoS ONE 2012, 7, e37135. [Google Scholar] [CrossRef] [PubMed]
- Catchen, J.; Hohenlohe, P.A.; Bassham, S.; Amores, A.; Cresko, W.A. Stacks: An Analysis Tool Set for Population Genomics. Mol. Ecol. 2013, 22, 3124–3140. [Google Scholar] [CrossRef] [PubMed]
- Zheng, X.; Levine, D.; Shen, J.; Gogarten, S.M.; Laurie, C.; Weir, B.S. A High-Performance Computing Toolset for Relatedness and Principal Component Analysis of SNP Data. Bioinformatics 2012, 28, 3326–3328. [Google Scholar] [CrossRef] [PubMed]
- Malinsky, M.; Trucchi, E.; Lawson, D.J.; Falush, D. RADpainter and fineRADstructure: Population Inference from RADseq Data. Mol. Biol. Evol. 2018, 35, 1284–1290. [Google Scholar] [CrossRef] [PubMed]
- White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols; Elsevier: Amsterdam, The Netherlands, 1990; pp. 315–322. ISBN 978-0-12-372180-8. [Google Scholar]
- Downie, S.R.; Katz-Downie, D.S. A Molecular Phylogeny of Apiaceae Subfamily Apioideae: Evidence from Nuclear Ribosomal DNA Internal Transcribed Spacer Sequences. Am. J. Bot. 1996, 83, 234–251. [Google Scholar] [CrossRef]
- Huelsenbeck, J.P.; Ronquist, F.; Nielsen, R.; Bollback, J.P. Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science 2001, 294, 2310–2314. [Google Scholar] [CrossRef]
- Anderson, M.J. A New Method for Non-parametric Multivariate Analysis of Variance. Austral Ecol. 2001, 26, 32–46. [Google Scholar] [CrossRef]
- Oksanen, J.; Simpson, G.; Blanchet, F.; Kindt, R.; Legendre, P.; Minchin, P.; O’Hara, R.; Solymos, P.; Stevens, M.; Szoecs, E.; et al. Vegan: Community Ecology Package 2022. Available online: https://CRAN.R-project.org/package=vegan (accessed on 23 December 2023).
- Martinez Arbizu, P. PairwiseAdonis: Pairwise Multilevel Comparison Using Adonis. (R Package Version 0.4). 2020. Available online: https://github.com/pmartinezarbizu/pairwiseAdonis (accessed on 23 December 2023).
- De’ath, G. Multivariate Regression Trees: A New Technique for Modeling Species-Environment Relationships. Ecology 2002, 83, 1105–1117. [Google Scholar] [CrossRef]
Population | Colfiorito | Visso | Sologno | Peschici | Rotello | Lecce |
---|---|---|---|---|---|---|
Colfiorito | ||||||
Visso | 0.081952 | |||||
Sologno | 0.132106 | 0.111729 | ||||
Peschici | 0.554903 | 0.517516 | 0.605728 | |||
Rotello | 0.547273 | 0.510449 | 0.596142 | 0.060023 | ||
Lecce | 0.534588 | 0.499018 | 0.582669 | 0.073635 | 0.065404 |
Population | π | He | Ho |
---|---|---|---|
Colfiorito | 0.00211 | 0.00205 | 0.00193 |
Visso | 0.00248 | 0.00242 | 0.00237 |
Sologno | 0.00165 | 0.00161 | 0.00157 |
Peschici | 0.00153 | 0.00149 | 0.00127 |
Rotello | 0.00158 | 0.00154 | 0.00127 |
Lecce | 0.00156 | 0.00152 | 0.00147 |
Population | Site of Collection | Date of Collection | Longitudine | Latitudine | Elevation (m a.s.l.) | Distance from the Sea (km) |
---|---|---|---|---|---|---|
SOL | Sologno (RE) | 28 July 2020 | 32T0611040 | 4912096 | 803 | 44.84 |
COL | Colfiorito (PG) | 21 July 2020 | 33T0331639 | 4769280 | 773 | 70.45 |
VIS | Cupi di Visso (MC) | 14 July 2020 | 33T0346318 | 4762414 | 976 | 60.01 |
ROT | Rotello (CB) | 19 June 2020 | 33T0503253 | 4623847 | 211 | 19.66 |
PES | Peschici (FG) | 18 June 2020 | 33T0584720 | 4640487 | 67 | 3.87 |
LEC | Frigole (LE) | 25 June 2020 | 34T0266130 | 4477221 | 12 | 1.85 |
Type of Parameter | Code | Descriptive Parameters and Values | Unit of Measure |
---|---|---|---|
Whole plant | HoP1 | height of the main stem | cm |
HoP2 | maximum plant height | cm | |
NoLS | number of lateral branches | unit | |
NoL | number of leaves | unit | |
NoH | number of flower heads | unit | |
LoW | length of the stem wing (15) | mm | |
LoT | length of the spine of the stem wing (15) | mm | |
Leaves | NoLb | number of lobes per leaf | unit |
LoL | leaf length | mm | |
LoLLb | length of the longest lobe per each leaf | mm | |
WoLLb | width of the longest lobe per each leaf | mm | |
LoSLb | length of the shortest lobe per leaf | mm | |
WoSLb | width of the shortest lobe per leaf | mm | |
LOTL | length of the spine (6 per leaf) | mm | |
PoL | perimeter of the leaf | mm | |
AoL | area of the leaf | mm2 | |
CoL | circularity of the leaf | ratio | |
AroL | aspect ratio of the leaf | ratio | |
RoL | round of the leaf | ratio | |
SoL | solidity of the leaf | ratio | |
Flower heads | DoH | diameter | mm |
DoR | diameter of the receptacle | mm | |
ToR | thickness of the receptacle | mm | |
LoTB | length of the spine of the bract (5 per head) | mm | |
GHBH | glandular hairs on the bracts | Visual rating | |
TBH | trichomes on the bracts | Visual rating | |
Fruits | Area | Area | mm2 |
Perim | Perimeter | mm | |
Height | Height | mm | |
Width | Width | mm | |
AR | Aspect Ratio | ratio | |
Circ | Circularity | ratio | |
Mean | Medium gray | 8-bits |
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Casavecchia, S.; Giannelli, F.; Giovannotti, M.; Trucchi, E.; Carducci, F.; Quattrini, G.; Lucchetti, L.; Barucca, M.; Canapa, A.; Biscotti, M.A.; et al. Morphological and Genomic Differences in the Italian Populations of Onopordum tauricum Willd.—A New Source of Vegetable Rennet. Plants 2024, 13, 654. https://doi.org/10.3390/plants13050654
Casavecchia S, Giannelli F, Giovannotti M, Trucchi E, Carducci F, Quattrini G, Lucchetti L, Barucca M, Canapa A, Biscotti MA, et al. Morphological and Genomic Differences in the Italian Populations of Onopordum tauricum Willd.—A New Source of Vegetable Rennet. Plants. 2024; 13(5):654. https://doi.org/10.3390/plants13050654
Chicago/Turabian StyleCasavecchia, Simona, Francesco Giannelli, Massimo Giovannotti, Emiliano Trucchi, Federica Carducci, Giacomo Quattrini, Lara Lucchetti, Marco Barucca, Adriana Canapa, Maria Assunta Biscotti, and et al. 2024. "Morphological and Genomic Differences in the Italian Populations of Onopordum tauricum Willd.—A New Source of Vegetable Rennet" Plants 13, no. 5: 654. https://doi.org/10.3390/plants13050654