Published October 8, 2025 | Version v1

Pollen morphology and species differentiation in selected species of Inuleae (Asteraceae)

  • 1. Sichuan Normal University, Chengdu, China
  • 2. Henan Agricultural University, Zhengzhou, China
  • 3. Beijing Dayu Middle School, Beijing, China
  • 4. Sichuan Leshan Ecological Environment Monitoring Center Station, Leshan, China
  • 5. Institute of Botany, Chinese Academy of Sciences, Beijing, China

Description

The tribe Inuleae is widely distributed within Asteraceae and exhibits considerable morphological variation, which complicates species classification. Pollen morphology provides relatively stable features for species delimitation, yet comprehensive palynological data for many species remain limited. In this study, the pollen morphology of 19 species from eight genera of Inuleae was investigated using light microscopy (LM) and scanning electron microscopy (SEM), with a focus on 10 quantitative traits. Multivariate analyses, including principal component analysis (PCA) and hierarchical clustering analysis (HCA), showed that both pollen size and exine ornamentation contribute to interspecific differentiation. Differences were especially notable between Blumea and Carpesium, with the latter showing larger pollen grains and more slender, scattered spines. This research also presents first-time palynological descriptions of Blumea, Carpesium, Inula, Laggera, Pentanema, and Pterocaulon. Overall, the findings indicate that pollen morphological traits are informative for species differentiation and lay a foundation for further palynological classification within Inuleae.

Files

PK_article_165364.pdf

Files (8.5 MB)

Name Size Download all
md5:cd1026ebbd8e1169863778f6c9ee3f45
8.5 MB Preview Download

System files (248.4 kB)

Name Size Download all
md5:c75d64150c25e0b625204c85c6120f3e
248.4 kB Download

Linked records

Additional details

References

  • Anderberg AA (1989) Phylogeny and reclassification of the tribe Inuleae (Asteraceae). Canadian Journal of Botany 67: 2277–2296. https://doi.org/10.1139/b89-292
  • Anderberg AA (1991) Taxonomy and phylogeny of the tribe Inuleae (Asteraceae). Plant Systematics and Evolution 176: 75–123. https://doi.org/10.1007/BF00937947
  • Anderberg AA (2009) Inuleae. In: Funck VA, Susanna A, Stuessy TF, Bayer RJ (Eds) Systematics, Evolution, and Biogeography of Compositae. Sheridan Books Inc, Ann Arbor, 667–680.
  • Anderberg AA, Eldenäs P (2007) Inuleae. In: Kadereit JW, Jeffrey C (Eds) The Families and Genera of Vascular Plants Vol. 8. Flowering Plants Eudicots: Asterales. Springer, Berlin, 374–375.
  • Andrade C (2021) Z Scores, standard scores, and composite test scores explained. Indian Journal of Psychological Medicine 43: 555–557. https://doi.org/10.1177/02537176211046525
  • Bahadur S, Taj S, Long WQ, Ahmad M (2022) Pollen morphology and its implication in the taxonomy of some selected tribes of the Asteraceae of Hainan Island South China. Botanical Review 88: 271–298. https://doi.org/10.1007/s12229-022-09277-3
  • Becht E, McInnes L, Healy J, Dutertre CA, Kwok IWH, Ng LG, Ginhoux F, Newell EW (2019) Dimensionality reduction for visualizing single-cell data using UMAP. Nature Biotechnology 37: 38–44. https://doi.org/10.1038/nbt.4314
  • Blackmore S (2007) Pollen and spores: Microscopic keys to understanding the earth's biodiversity. Plant Systematics and Evolution 263: 3–12. https://doi.org/10.1007/s00606-006-0464-3
  • Bremer K (1987) Tribal interrelationships of the Asteraceae. Cladistics: The International Journal of the Willi Hennig Society 3: 210–253. https://doi.org/10.1111/j.1096-0031.1987.tb00509.x
  • Carrijo TT, Garbin ML, Picanço Leite W, Mendonça CBF, Esteves RL, Gonçalves-Esteves V (2013) Pollen morphology of some related genera of Vernonieae (Asteraceae) and its taxonomic significance. Plant Systematics and Evolution 299: 1275–1283. https://doi.org/10.1007/s00606-013-0795-9
  • Chen YS, Anderberg AA (2011a) Blumea DC. In: Wu ZY, Raven PH, Hong DY (Eds) Flora of China, Vol. 20–21. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, 829 pp.
  • Chen YS, Anderberg AA (2011b) Carpesium L. In: Wu ZY, Raven PH, Hong DY (Eds) Flora of China, Vol. 20–21. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis, 821 pp.
  • Chung I, Kim M, Moon H (2008) Antiplasmodial activity of sesquiterpene lactone from Carpesium rosulatum in mice. Parasitology Research 103: 341–344. https://doi.org/10.1007/s00436-008-0977-5
  • Chung KS, Elisens WJ, Skvarla JJ (2010) Pollen morphology and its phylogenetic significance in tribe Sanguisorbeae (Rosaceae). Plant Systematics and Evolution 285(3–4): 139–148. https://doi.org/10.1007/s00606-009-0262-9
  • Corrêa MVG, Lima LFP, Bauermann SG (2008) Morfologia polínica das espécies brasileiras de Pterocaulon Ell. (Asteraceae). Pesquisas. Série Botânica (59): 263–276.
  • Coutinho AP, Aguiar CF, Bandeira DSD, Dinis AM (2011) Comparative pollen morphology of the Iberian species of Pulicaria (Asteraceae, Inuleae, Inulinae) and its taxonomic significance. Plant Systematics and Evolution 297: 171–183. https://doi.org/10.1007/s00606-011-0505-4
  • Coutinho AP, Silveira P, Pita C, Santos MJ, Saraiva C, Perpétuo NC (2020) Pollen morphology of Xanthium L. (s.l.) (Asteraceae, Asteroideae, Heliantheae, Ambrosiinae) in the Iberian Peninsula – a palynotaxonomic approach to a poisonous, allergenic and invasive genus. Grana 60(1): 35–56. https://doi.org/10.1080/00173134.2020.1737729
  • Ďurišová Ľ, Ďúranová H, Kšiňan S, Ernst D, Šebesta M, Žitniak Čurná V, Eliáš P, Qian Y, Straka V, Feng H, Tomovičová L, Kotlárová N, Kratošová G, Kolenčík M (2023) Exploring the impact of metal-based nanofertilizers: A case study on sunflower pollen morphology and yield in field conditions. Agronomy (Basel) 13(12): 2922. https://doi.org/10.3390/agronomy13122922
  • Ejsmond MJ, Wrońska-Pilarek D, Ejsmond A, Dragosz-Kluska D, Karpińska-Kołaczek M, Kołaczek P, Kozłowski J (2011) Does climate affect pollen morphology? Optimal size and shape of pollen grains under various desiccation intensity. Ecosphere 2(10): 1–15. https://doi.org/10.1890/ES11-00147.1
  • El-Ghazaly G, Anderberg AA (1995) Pollen morphology of Phagnalon and Aliella (Asteraceae, Gnaphalieae) and its taxonomical implications. Grana 34(2): 89–99. https://doi.org/10.1080/00173139509429999
  • Erb S, Graf E, Zeder Y, Lionetti S, Berne A, Clot B, Lieberherr G, Tummon F, Wullschleger P, Crouzy B (2024) Real-time pollen identification using holographic imaging and fluorescence measurements. Atmospheric Measurement Techniques 17(2): 441–451. https://doi.org/10.5194/amt-17-441-2024
  • Erdtman G (1952) Pollen morphology and plant taxonomy: angiosperms. Almqvist & Wiksell, Stockholm. https://doi.org/10.1080/11035895209453507
  • Erdtman G (1960) The acetolysis method, a revised description. Svensk Botanisk Tidskrift 54: 561–564.
  • Erdtman G (1969) Handbook of palynology, morphology, taxonomy, ecology. An introduction to the study of pollen grains and spores. Hafner Pub, New York.
  • Ferguson IK (1985) The role of pollen morphology in plant systematics. Anales de la Asociación de Palinólogos de Lengua Española 2: 5–18.
  • Fu ZX, Jiao BH, Nie B, Zhang GJ, Gao TG (2016) A comprehensive generic-level phylogeny of the sunflower family: Implications for the systematics of Chinese Asteraceae. Journal of Systematics and Evolution 54(4): 416–437. https://doi.org/10.1111/jse.12216
  • Gabarayeva NI, Britski DA, Grigorjeva VV (2024) Pollen wall development in Impatiens glandulifera: Exine substructure and underlying mechanisms. Protoplasma 261: 111–124. https://doi.org/10.1007/s00709-023-01887-x
  • Gagnepain MF (1920) Un genre nouveau de Composées, Blumeopsis. Bulletin du Muséum National d'Histoire Naturelle 26: 75–76.
  • Halbritter H, Silvia U, Grímsson F, Weber M, Zetter R, Hesse M, Buchner R, Svojtka M, Frosch-Radivo A (2018) Illustrated Pollen Terminology. Springer, Cham, Switzerland, 483 pp. https://doi.org/10.1007/978-3-319-71365-6
  • Heidarian M, Masoumi SM, Amiri S (2021) Palynological study on selected species from Hyacinthaceae with focus on taxonomical implications in Iran. Palynology 46(1): 1–16. https://doi.org/10.1080/01916122.2021.1952329
  • Hesse M, Blackmore S (2013) Preface to the special focus manuscripts. Plant Systematics and Evolution 299: 1011–1012. https://doi.org/10.1007/s00606-013-0811-0
  • Huang Y, An YM, Meng SY, Guo YP, Rao GY (2017) Taxonomic status and phylogenetic position of Phaeostigma in the subtribe Artemisiinae (Asteraceae). Journal of Systematics and Evolution 55(5): 426–436. https://doi.org/10.1111/jse.12257
  • Huang XK, Wu R, Xiong Z, Ma ZH (2023) Pollen morphology of Clerodendrum L. (Lamiaceae) from China and its systematic implications. PhytoKeys 235: 53–68. https://doi.org/10.3897/phytokeys.235.111516
  • Jardine PE, Palazzesi L, Tellería MC, Barreda VD (2022) Why does pollen morphology vary? Evolutionary dynamics and morphospace occupation in the largest angiosperm order (Asterales). The New Phytologist 234(3): 1075–1087. https://doi.org/10.1111/nph.18024
  • Jia M, Li X (2005) Chinese national pharmacology, 1st ed. Chinese Medical Science Press, Beijing.
  • Jia PF, Li HJ, Yang WC (2017) Transmission electron microscopy (TEM) to study histology of pollen and pollen tubes. In: Schmidt A (Ed.) Plant Germline Development, Vol. 1669. Humana Press, New York, 181–189. https://doi.org/10.1007/978-1-4939-7286-9_15
  • Kadluczka D, Sliwinska E, Grzebelus E (2022) Combining genome size and pollen morphology data to study species relationships in the genus Daucus (Apiaceae). BMC Plant Biology 22: 1–13. https://doi.org/10.1186/s12870-022-03743-1
  • Karlıoğlu Kılıç N, Yılmaz Dağdeviren R, Paksoy MY, Tuncalı Yaman T (2021) Pollen morphology of eight endemic Inula L.(Asteraceae) species in Turkey. Palynology 45(2): 235–244. https://doi.org/10.1080/01916122.2020.1784306
  • Keating JN, Garwood RJ, Sansom RS (2023) Phylogenetic congruence, conflict and consilience between molecular and morphological data. BMC Ecology and Evolution 23: 30. https://doi.org/10.1186/s12862-023-02131-z
  • Kim KJ, Jansen RK (1995) NdhF sequence evolution and the major clades in the sunflower family. Proceedings of the National Academy of Sciences of the United States of America 92(22): 10379–10383. https://doi.org/10.1073/pnas.92.22.10379
  • Kim DK, Baek NI, Choi SU, Lee CO, Lee KR, Zee OP (1997) Four new cytotoxic germacranolides from Carpesium divaricatum. Journal of Natural Products 60(11): 1199–1202. https://doi.org/10.1021/np970157d
  • Larson DA, Skvarla JJ (1962) An electron microscope study of exine stratification and fine structure. Pollen et Spores 4: 233–246.
  • Leins P (1971) Pollensystematische studien an Inuleen, I: Tarchonanthineae, Plucheinae, Inulinae, Buphthalminae. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 91: 91–146.
  • Li WW, Wang YN, Liu LQ, Niu YY, Zhao SR, Zhang SK, Wang YT, Liao K (2021) Pollen morphology of selected apricot (Prunus) taxa. Palynology 45(1): 95–102. https://doi.org/10.1080/01916122.2020.1737260
  • Lin M, Qiu J, Xie K, Tan D (2023) Palynological features and taxonomic significance for 16 species of Gagea (Liliaceae) from Xinjiang, China. PhytoKeys 225: 53–68. https://doi.org/10.3897/phytokeys.225.101518
  • Lu L, Fritsch PW, Wang H, Li HT, Li DZ, Chen JQ (2009) Pollen morphology of Gaultheria L. and related genera of subfamily Vaccinioideae: Taxonomic and evolutionary significance. Review of Palaeobotany and Palynology 154(1–4): 106–123. https://doi.org/10.1016/j.revpalbo.2008.12.009
  • Lu KQ, Xie G, Li M, Li JF, Trivedi A, Ferguson DK, Yao YF, Wang YF (2018) Dataset of pollen morphological traits of 56 dominant species among desert vegetation in the eastern arid central Asia. Data in Brief 18: 1022–1046. https://doi.org/10.1016/j.dib.2018.03.122
  • Lu LL, Jiao BH, Qin F, Xie G, Lu KQ, Li JF, Sun B, Li M, Ferguson DK, Gao TG, Yao YF, Wang YF (2022) Artemisia pollen dataset for exploring the potential ecological indicators in deep time. Earth System Science Data 14(9): 3961–3995. https://doi.org/10.5194/essd-14-3961-2022
  • Maciejewska-Rutkowska I, Bocianowski J, Wrońska-Pilarek D (2021) Correction: Pollen morphology and variability of Polish native species from genus Salix L. PLOS ONE 16: e0252253. https://doi.org/10.1371/journal.pone.0252253
  • Magenta MAG, Nunes ADD, Mendonça CBF, Gonçalves-Esteves V (2010) Palynotaxonomy of Brazilian Viguiera (Asteraceae) species. Boletín de La Sociedad Argentina de Bátanica 45: 285–299.
  • Marques D, Pico GMV, Nakajima JN, Dematteis M (2021) Pollen morphology and its systematic value to southern South American species of Lepidaploa (Vernonieae: Asteraceae). Rodriguésia 72: 1–18. https://doi.org/10.1590/2175-7860202172017
  • McInnes L, Healy J, Melville J (2018) Uniform manifold approximation and projection for dimension reduction. arXiv, 1802.03426. https://doi.org/10.48550/arXiv.1802.03426
  • Meo AA, Khan MA (2009) Pollen morphology of rare taxa Laggera alata and its related species Pluchea lanceolata of tribe Plucheeae (Asteraceae). Pakistan Journal of Botany 41: 1539–1544.
  • Merxmüller H, Leins P, Roessler H (1977) Inuleae – Systematic review. In: Heywood VH, Harborne JB, Turner BL (Eds) The Biology and Chemistry of the Compositae, Vol. 1. Academic Press, London, 577–602.
  • Mo RG, Bai XL, Ma YY, Cao R (1997) On the intraspecific variations of pollen morphology and pollen geography of a relic species – Helianthemum songaricum Schrenk. Xibei Zhiwu Xuebao 17(4): 528–532.
  • Moon H (2007) Antiplasmodial activity of ineupatorolides A from Carpesium rosulatum. Parasitology Research 100: 1147–1149. https://doi.org/10.1007/s00436-006-0369-7
  • Moon H, Zee O (2011) Sesquiterpene lactones from Carpesium rosulatum with potential cytotoxicity against five human cancer cell lines. Human & Experimental Toxicology 30: 1083–1087. https://doi.org/10.1177/0960327110386818
  • Nowicke JW, Skvarla JJ (1979) Pollen morphology: The potential influence in higher order systematics. Annals of the Missouri Botanical Garden 66(4): 633–700. https://doi.org/10.2307/2398914
  • Nylinder S, Anderberg AA (2015) Phylogeny of the Inuleae (Asteraceae) with special emphasis on the Inuleae‐Plucheinae. Taxon 64(1): 110–130. https://doi.org/10.12705/641.22
  • Osman AK (2006) Contributions to the pollen morphology of the tribe Inuleae (subfamily Asteroideae‐Compositae) in the flora of Egypt. Feddes Repertorium 117(3–4): 193–206. https://doi.org/10.1002/fedr.200511096
  • Osman AK (2011) Pollen morphology of tribes Gnaphalieae, Helenieae, Plucheeae and Senecioneae (subfamily Asteroideae) of Compositae from Egypt. American Journal of Plant Sciences 2(2): 120–133. https://doi.org/10.4236/ajps.2011.22014
  • Peng Y, Pu X, Yu Q, Zhou H, Huang T, Xu B, Gao X (2023) Comparative pollen morphology of selected species of Blumea DC. and Cyathocline Cass. and its taxonomic significance. Plants 12(16): 2909. https://doi.org/10.3390/plants12162909
  • Pereira Coutinho A, Dinis AM (2007) A contribution to the ultrastructural knowledge of the pollen exine in subtribe Inulinae (Inuleae, Asteraceae). Plant Systematics and Evolution 269: 159–170. https://doi.org/10.1007/s00606-007-0585-3
  • Pereira Coutinho A, Dinis AM (2009) A light, scanning electron and transmission electron microscopic study of pollen wall architecture in the subtribe Gnaphaliinae (Gnaphalieae, Asteraceae). Plant Systematics and Evolution 283: 79–92. https://doi.org/10.1007/s00606-009-0216-2
  • Perveen A (1999) Contributions to the pollen morphology of the family Compositae. Turkish Journal of Biology = Türk Biyoloji Dergisi 23: 523–536. https://journals.tubitak.gov.tr/biology/vol23/iss4/15/
  • Pornpongrungrueng P, Borchsenius F, Englund M, Anderberg AA, Gustafsson MHG (2007) Phylogenetic relationships in Blumea (Asteraceae: Inuleae) as evidenced by molecular and morphological data. Plant Systematics and Evolution 269: 223–243. https://doi.org/10.1007/s00606-007-0581-7
  • Pornpongrungrueng P, Gustafsson MHG, Borchsenius F, Koyama H, Chantaranothai P (2016) Blumea (Compositae: Inuleae) in continental Southeast Asia. Kew Bulletin 71(1): 1. https://doi.org/10.1007/s12225-016-9612-2
  • Punt W, Hoen PP, Blackmore S, Nilsson S, Thomas LA (2007) Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143(1–2): 1–81. https://doi.org/10.1016/j.revpalbo.2006.06.008
  • Qu TM, Xie G, Zheng XY, Chen XY, Zhang YR, Lu LL, Fu ZX (2025) Systematic analysis of some Astereae (Asteraceae) species by integrating pollen morphology and molecular evidence. Frontiers in Plant Science 16: 1558995. https://doi.org/10.3389/fpls.2025.1558995
  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/
  • Skvarla JJ, Turner BL, Patel VC, Tomb AS, Thanikaimoni G (1977) Pollen morphology in the Compositae and in morphologically related families. In: Heywood VH, Harborne JB, Turner BL (Eds) The Biology and Chemistry of the Compositae. Academic Press, London, 141–265.
  • Skvarla JJ, DeVore ML, Chissoe WF (2005) Lophate sculpturing of Vernonieae (Compositae) pollen. Review of Palaeobotany and Palynology 133(1–2): 51–68. https://doi.org/10.1016/j.revpalbo.2004.09.001
  • Tanaka N, Uehara K, Murata J (2004) Correlation between pollen morphology and pollination mechanisms in the Hydrocharitaceae. Journal of Plant Research 117: 265–276. https://doi.org/10.1007/s10265-004-0155-5
  • Usma A, Ahmad M, Zafar M, Sultana S, Ullah F, Saqib S, Ayaz A, Zaman W (2022) Palynological study of weed flora from Potohar Plateau. Agronomy (Basel) 12(10): 2500. https://doi.org/10.3390/agronomy12102500
  • Wang FX, Qian NF, Zhang YL, Yang HQ (1995) Pollen morphology of Chinese plants, 2nd ed. Science Press, Beijing.
  • Wang H, Yu WB, Chen JQ, Blackmore S (2009) Pollen morphology in relation to floral types and pollination syndromes in Pedicularis (Orobanchaceae). Plant Systematics and Evolution 277: 153–162. https://doi.org/10.1007/s00606-008-0112-1
  • Wodehouse RP (1935) Pollen grains. McGraw-Hill Book Company, New York, 574 pp.
  • Wortley AH, Funk VA, Robinson H, Skvarla JJ, Blackmore S (2007) A search for pollen morphological synapomorphies to classify rogue genera in Compositae (Astera­ceae). Review of Palaeobotany and Palynology 146(1–4): 169–181. https://doi.org/10.1016/j.revpalbo.2007.03.003
  • Wrońska-Pilarek D, Jagodziński AM, Bocianowski J, Janyszek M (2015) The optimal sample size in pollen morphological studies using the example of Rosa canina L. (Rosaceae). Palynology 39(1): 56–75. https://doi.org/10.1080/01916122.2014.933748
  • Ye WP, Min J, Ren K, Yang F, Li W, Chen P, Fang AP (2015) Origin 9.1 Scientific Graphing and Data Analysis. China Machine Press, Beijing.
  • Zarin P, Ghahremaninejad F, Maassoumi AA (2010) Comparative anatomy and pollen features of Amblyocarpum and Carpesium (Asteracerae: Inuleae) in Iran. Iranian Journal of Botany 16: 49–53.
  • Zarrei M, Zarre S (2005) Pollen morphology of the genus Gagea (Liliaceae) in Iran. Flora 200(1): 96–108. https://doi.org/10.1016/j.flora.2004.04.001
  • Zhang YN, Qian C (2011) SEM observation on pollen morphology of lily species. Caoye Xuebao 20: 111–118.
  • Zhang XP, Zhou ZZ (2016) Pollen morphology and phylogeny of the tribe Astereae (Compositae). University of Science and Technology of China Press, Anhui.
  • Zhang JP, Wang GW, Tian XH, Yang YX, Liu QX, Chen LP, Li HL, Zhang WD (2015) The genus Carpesium: A review of its ethnopharmacology, phytochemistry and pharmacology. Journal of Ethnopharmacology 163: 173–191. https://doi.org/10.1016/j.jep.2015.01.027
  • Zhang WX, Zhao MM, Fan JJ, Zhou T, Chen YX, Cao FL (2017) Study on relationship between pollen exine ornamentation pattern and germplasm evolution in flowering crabapple. Scientific Reports 7: 39759. https://doi.org/10.1038/srep39759
  • Zhang YB, Yuan Y, Pang YX, Yu FL, Yuan C, Wang D, Hu X (2019) Phylogenetic reconstruction and divergence time estimation of Blumea DC. (Asteraceae: Inuleae) in China based on nrDNA ITS and cpDNA trnL-F sequences. Plants 8(7): 210. https://doi.org/10.3390/plants8070210
  • Zhao Z, Skvarla JJ, Jansen RK, DeVore ML (2000) Phylogenetic implications of pollen morphology and ultrastructure in the Barnadesioideae (Asteraceae). Lundellia 2000(3): 26–40. https://doi.org/10.25224/1097-993X-3.1.26