Abstract
Elaborate petals are highly diverse in morphology, structure, and epidermal differentiation and play a key role in attracting pollinators. There have been few studies on the elaborate structure of petals in the tribe Isopyreae (Ranunculaceae). Seven genera in Isopyreae (Aquilegia, Semiaquilegia, Urophysa, Isopyrum, Paraquilegia, Dichocarpum, and Leptopyrum) have petals that vary in morphology, and two genera (Enemion and Thalictrum) have no petals. The petals of nine species belonged to 7 genera in the tribe were studied to reveal their nectary structure, epidermal micromorphology and ancestral traits. The petal nectaries of Isopyreae examined in this study were located at the tip of spurs (Aquilegia yabeana and A. rockii), or the bottom of shallow sacs (Semiaquilegia adoxoides, Urophysa henryi, Isopyrum manshuricum, and Paraquilegia microphylla), a cup-shaped structure (Dichocarpum fargesii) and a bilabiate structure (Leptopyrum fumarioides). The petal nectary of eight species in Isopyreae (except A. ecalcarata) was composed of secretory epidermis, nectary parenchyma, and vascular tissues, and some sieve tubes reached the secretory parenchyma cells. Among the eight species with nectaries examined in the present study, A. yabeana had the most developed nectaries, with 10–15 layers of secretory parenchyma cells. The epidermal cells of mature petals of the nine species were divided into 11 types. Among these 11 types, there were two types of secretory cells and two types of trichomes. Aquilegia yabeana and A. rockii had the highest number of cell types (eight types), and I. manshuricum and L. fumarioides had the lowest number of cell types (three types). Aquilegia ecalcarata had no secretory cells, and the papillose conical polygonal secretory cells of D. fargesii were different from those of the other seven species with nectaries. Trichomes were found only in Aquilegia, Semiaquilegia, Urophysa, and Paraquilegia. The ancestral mode of nectar presentation in Isopyreae was petals with hidden nectar (70.58%). The different modes of nectar presentation in petals may reflect adaptations to different pollinators in Isopyreae.
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References
Ali MA, Al-Hemaid FM (2011) Taxonomic significance of trichomes micromorphology in cucurbits. Saudi J Biol Sci 18:87–92. https://doi.org/10.1016/j.sjbs.2010.10.003
Antoń S, Kamińska M (2015) Comparative floral spur anatomy and nectar secretion in four representatives of Ranunculaceae. Protoplasma 252:1587–1601. https://doi.org/10.1007/s00709-015-0794-5
Ballerini ES, Min Y, Edwards MB, Kramer EM, Hodges SA (2020) POPOVICH, encoding a C2H2 zinc-finger transcription factor, plays a central role in the development of a key innovation, floral nectar spurs Aquilegia. Proc Natl Acad Sci 117(36):22552–22560. https://doi.org/10.1073/pnas.2006912117
Endress PK, Matthews ML (2006) Elaborate petals and staminodes in eudicots: Diversity, function, and evolution. Organisms Diversity Evol 6:257–293. https://doi.org/10.1016/j.ode.2005.09.005
Erbar C, Kusma S, Leins P (1998) Development and interpretation of nectary organs in Ranunculaceae. Flora 194:317–332. https://doi.org/10.1016/S0367-2530(17)30920-9
Christensen K, Hansen H (1998) SEM-studies of epidermal patterns of petals in the angiosperms. Opera Botanica 135:1–91
Costa VBSD, Pimentel RMM, Chagas MGS, Alves GD, Castro CCD (2017) Petal micromorphology and its relationship to pollination. Plant Biol 19(2):115–122. https://doi.org/10.1111/plb.12523
Fior S, Li MA, Oxelman B, Viola R, Hodges SA, Ometto L, Varotto C (2013) Spatiotemporal reconstruction of the Aquilegia rapid radiation through next-generation sequencing of rapidly evolving cpDNA Regions. New Phytol 198:579–592. https://doi.org/10.1111/nph.12163
Fu XH, Shan HY, Yao X, Cheng J, Jiang YC, Yin XF, Kong HZ (2022) Petal development and elaboration. J Exp Bot 73(11):3308–3318. https://doi.org/10.1093/jxb/erac092
Kalyaanamoorthy S, Minh BQ, Wong TKF, Haeseler AV, Jermiin LS (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84. https://doi.org/10.1111/j.1095-8339.1981.tb00129.x
Lewis PO (2001) A likelihood approach to estimating phylogeny fromdiscrete morphological character data. Syst Biol 50(6):913–925. https://doi.org/10.1080/106351501753462876
Luo MR (2019) Floral morphogenesis in Leptopyrum (Ranunculaceae) with scanning electron microscopy. Guihaia 40(11):1645–1652. https://doi.org/10.11931/guihaia.gxzw201903007
Luo MR, Zhang J (2020) Floral organogenesis in Semiaquilegia (Ranunculaceae) with scanning electron microscopy. Acta Botan Boreali-Occiden Sin 40(11):1874–1880
Maddison WP, Maddison DR (2021) Mesquite: a modular system for evolutionary analysis. version: 3.61.[EB/OL]. https://mesquiteproject.org/
Ojeda I, Francisco-Ortega J, Cronk QC (2009) Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Ann Bot 104:1099–1110. https://doi.org/10.1093/aob/mcp211
Piwowarczyk R, Kasińska J (2017) Petal epidermal micromorphology in holoparasitic Orobanchaceae and its significance for systematics and pollination ecology. Austral Syst Bot 30:48–63. https://doi.org/10.1071/SB16028
Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149. https://doi.org/10.1038/334147a0
Ren Y, Gu TQ, Chang HL (2011) Floral development of Dichocarpum, Thalictrum, and Aquilegia (Thalictroideae, Ranunculaceae). Plant Syst Evol 292:203–213 (https://www.jstor.org/stable/43558161)
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Rysiak K, Żuraw B (2011) The biology of flowering of winter aconite (Eranthis hyemalis (L.) Salisb.). Acta Agrobot 64(2):25–32. https://doi.org/10.5586/aa.2011.014
Seyedi Z, Salmaki Y (2015) Trichome morphology and its significance in the systematics of Phlomoides (Lamiaceae; Lamioideae; Phlomideae). Flora 213:40–48. https://doi.org/10.1016/j.flora.2015.04.003
Sun L (2014) Study on the breeding system and pollination biology of three species of Isopyreae (Ranunculaceae). MD Thesis, Shaanxi normal university
Sun L, Ren Y (2016) Pollinator-mediated selection on nectary depth in Urophysa (Ranunculaceae). Modern Phytomorphol 9(suppl):83. https://doi.org/10.5281/zenodo.159708
Tamura MN (1966) Morphology, ecology and phylogeny of the Ranunculaceae VI. Sci Rep Osaka Univ 15:13–35
Tamura MN (1967) Morphology, ecology and phylogeny of the Ranunculaceae VII. Sci Rep Osaka Univ 16:21–43
Tamura MN (1968) Morphology, ecology and phylogeny of the Ranunculaceae VIII. Sci Rep Osaka Univ 17:41–56
Thairu MW, Johanne B (2015) The role of pollinators in maintaining variation in flower colour in the Rocky Mountain columbine Aquilegia Coerulea. Ann Bot 115(6):971–979. https://doi.org/10.1093/aob/mcv028
The angiosperm phylogeny group (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181(1):1–20. https://doi.org/10.1111/boj.12385
Thien LB, Bernhardt P, Devall MS, Chen ZD, Luo YB, Fan JH, Yuan LC, Williams JH (2009) Pollination biology of basal angiosperms (ANITA grade). Amer J Bot 96(1):166–182. https://doi.org/10.3732/ajb.0800016
Tian M (2019) Study on the adaptation of seven species of Ranunculaceae to pollinators by different nectar hiding modes. MD Thesis, Shaanxi normal university
Tian M, Ren Y (2019) Evolutionary significance of discrete functional adaptations to pollinators in generalist flowers: a case study of three species of Ranunculus s.l. (Ranunculaceae) with distinct petal nectary scales. Bot J Linn Soc 189(3):281–292. https://doi.org/10.1093/botlinnean/boy073
Timerman D, Barrett SCH (2018) Divergent selection on the biomechanical properties of stamens under wind and insect pollination. Proc R Soc B 285(1893). https://doi.org/10.1098/rspb.2018.2251
Timerman D, Barrett SCH (2019) Comparative analysis of pollen release biomechanics in Thalictrum: implications for evolutionary transitions between animal and wind pollination. New Phytol 224(3):1121–1132. https://doi.org/10.1111/nph.15978
Tucker SC, Hodges SA (2005) Floral ontogeny of Aquilegia, Semiaquilegia, and Enemion (Ranunculaceae). Int J Pl Sci 166(4):557–574 (https://www.jstor.org/stable/10.1086/429848)
Wang W, Lu AM, Ren Y, Endress ME, Chen ZD (2009) Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data. Perspect Pl Ecol Evol Syst 11(2):81–110. https://doi.org/10.1016/j.ppees.2009.01.001
Wang W, Wang HY, Dong JH, Zhang TJ, Xiao HX (2021) Comparative chloroplast genomes and phylogenetic analysis of Aquilegia. Appl Plant Sci 9(3):e11412. https://doi.org/10.1002/aps3.11412
Wang WC, Fu DZ, Li LQ, Bartholomew B, Brach AR, Dutton BE, Gilbert MG, Kadota Y, Robinson OR, Tamura M, Warnock MJ, Zhu GH, Ziman SN (2001) Ranunculaceae. Flora of China. In: Wu ZY, Raven PH, Hong DY. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis 6:133–438. http://www.iplant.cn/foc/pdf/Ranunculaceae.pdf
Whitney HM, Bennett KMV, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (2011) Why do so many petals have conical epidermal cells? Ann Bot 108:609–616. https://doi.org/10.1093/aob/mcr065
Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009a) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19(11):948–953. https://doi.org/10.1016/j.cub.2009.04.051
Whitney HM, Federle W, Glover BJ (2009b) Grip and slip: mechanical interactions between insects and the epidermis of flowers and flower stalks. Commun Integr Biol 19:1–6. https://doi.org/10.4161/cib.2.6.9479
Whitney HM, Kolle M, Andrew P, Chittka L, Steiner U, Glover BJ (2009c) Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science 323(5910):130–133. https://doi.org/10.1126/science.1166256
Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–711. https://doi.org/10.1038/nature05857
Whittemore AT (1997) Aquilegia. Flora of North America north of Mexico. In: Flora of North America Editorial Committee, Flora of North America Editorial Committee. Oxford University Press, New York 3:249–258. http://beta.floranorthamerica.org/Aquilegia
Xiang CL, Dong ZH, Peng H, Liu ZW (2010) Trichome micromorphology of the East Asiatic genus Chelonopsis (Lamiaceae) and its systematic implications. Flora 205:434–441. https://doi.org/10.1016/j.flora.2009.12.007
Yao X, Zhang WG, Duan XS, Yuan Y, Zhang R, Shan HY, Kong HZ (2019) The making of elaborate petals in Nigella through developmental repatterning. New Phytol 223:385–396. https://doi.org/10.1111/nph.15799
Yant L, Collani S, Puzey J, Levy C, Kramer EM (2015) Molecular basis for three-dimensional elaboration of the Aquilegia petal spur. Rroc R Soc 282:20142778. https://doi.org/10.1098/rspb.2014.2778
Zhai W, Duan XS, Zhang R, Guo CC, Li L, Xu GX, Shan HY, Kong HZ, Ren Y (2019) Chloroplast genomic data provide new and robust insights into the phylogeny and evolution of the Ranunculaceae. Molec Phylogen Evol 135:12–21. https://doi.org/10.1016/j.ympev.2019.02.024
Zhang D, Gao FL, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020a) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 20:348–355. https://doi.org/10.1111/1755-0998.13096
Zhang R, Min Y, Holappa LD, Walcher-Chevillet CL, Duan XS, Donaldson E, Kong HZ, Kramer EM (2020b) A role for the auxin response factors ARF6 and ARF8 homologs in petal spur elongation and nectary maturation in Aquilegia. New Phytol 227(5):1392–1405. https://doi.org/10.1111/nph.16633
Acknowledgements
We are very grateful to Mr. Guo-Yun Zhang of the State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, for assistance with scanning electron microscopy. We are very grateful to Mr. Meng Han for collecting materials of Aquilegia and Ms. Chun-qian Ren for ancestral state reconstruction analysis.
Funding
This work was supported by the National Natural Science Foundation of China (Nos. 31770203, 31100141) and the Fundamental Research Funds for the Central Universities (No. GK202002011).
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Xiao-hui Zhang designed the research and critically revised the work. Qing-qing Zhu contributed to data analysis and wrote the manuscript. All authors read and approved the manuscript.
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Supplementary file1. Figure S1 The phylogenetic tree constructed based on complete chloroplast genomes. Numbers on branches are bootstrap supports. (JPG 1465 KB)
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Supplementary file2. Figure S2 Evolution of nectar presentation modes in Isopyreae. (JPG 363 KB)
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Zhu, QQ., Xue, C., Sun, L. et al. The diversity of elaborate petals in Isopyreae (Ranunculaceae): a special focus on nectary structure. Protoplasma 260, 437–451 (2023). https://doi.org/10.1007/s00709-022-01787-6
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DOI: https://doi.org/10.1007/s00709-022-01787-6