215
Pollen mo phology and species di e en ia ion in selec ed
species o Inuleae (As e aceae)
Tianmeng Qu1,2 , Xinyu Chen2, Xinyi Zheng2, Yan u Zhang2, Yizhen Shao3, Hongze Sun4,
Bing Zhang5, Gan Xie6, Zhixi Fu1,2,7
1 Key Labo a o y o Land Resou ces E alua ion and Moni o ing in Sou hwes , Sichuan No mal Uni e si y, Minis y o Educa ion, Chengdu 610066, China
2 College o Li e Sciences, Sichuan No mal Uni e si y, Chengdu 610101, China
3 College o Li e Science, Henan Ag icul u al Uni e si y, Zhengzhou 450000, China
4 Beijing Dayu Middle School, Beijing 102300, China
5 Sichuan Leshan Ecological En i onmen Moni o ing Cen e S a ion, Leshan 614099, China
6 Big Da a and AI Resea ch Cen e o Biodi e si y Conse a ion, Ins i u e o Bo any, Chinese Academy o Sciences, Beijing 100093, China
7 Sus ainable De elopmen Resea ch Cen e o Resou ces and En i onmen o Wes e n Sichuan, Sichuan No mal Uni e si y, Chengdu, China
Co esponding au ho s: Gan Xie ([email p o ec ed]); Zhixi Fu ([email p o ec ed])
Copy igh : © Tianmeng Qu e al.
This is an open access a icle dis ibu ed unde
e ms o he C ea i e Commons A ibu ion
License (A ibu ion 4.0 In e na ional – CC BY 4.0).
Resea ch A icle
Abs ac
The ibe Inuleae is widely dis ibu ed wi hin As e aceae and exhibi s conside able
mo phological a ia ion, which complica es species classi ica ion. Pollen mo phology
p o ides ela i ely s able ea u es o species delimi a ion, ye comp ehensi e palyno-
logical da a o many species emain limi ed. In his s udy, he pollen mo phology o 19
species om eigh gene a o Inuleae was in es iga ed using ligh mic oscopy (LM) and
scanning elec on mic oscopy (SEM), wi h a ocus on 10 quan i a i e ai s. Mul i a i-
a e analyses, including p incipal componen analysis (PCA) and hie a chical clus e ing
analysis (HCA), showed ha bo h pollen size and exine o namen a ion con ibu e o
in e speci ic di e en ia ion. Di e ences we e especially no able be ween Blumea and
Ca pesium, wi h he la e showing la ge pollen g ains and mo e slende , sca e ed
spines. This esea ch also p esen s i s - ime palynological desc ip ions o Blumea, Ca -
pesium, Inula, Lagge a, Pen anema, and P e ocaulon. O e all, he indings indica e ha
pollen mo phological ai s a e in o ma i e o species di e en ia ion and lay a ounda-
ion o u he palynological classi ica ion wi hin Inuleae.
Key wo ds: Blumea, Ca pesium, HCA, palynology, PCA, SEM, axonomy
In oduc ion
Inuleae (As e aceae: As e oideae), sensu Ande be g and Eldenäs (2007),
comp ises app oxima ely 690 species in 66 gene a and ep esen s a majo
lineage o he amily. Mos species a e subsh ubs, sh ubs, o pe ennial he bs,
mainly adap ed o wa m o empe a e clima es, and he ibe is p ima ily dis-
ibu ed in Eu asia, wi h addi ional occu ences in No h A ica, Asia, and adja-
cen A abia (Ande be g 1989, 1991, 2009; Ande be g and Eldenäs 2007; Po n-
pong ung ueng e al. 2007). The ibe exhibi s conside able mo phological
Academic edi o : Alexande Sukho uko
Recei ed:
16 July 2025
Accep ed:
7 Sep embe 2025
Published:
8 Oc obe 2025
Ci a ion: Qu T, Chen X, Zheng X, Zhang
Y, Shao Y, Sun H, Zhang B, Xie G, Fu Z
(2025) Pollen mo phology and species
di e en ia ion in selec ed species o
Inuleae (As e aceae). Phy oKeys 263:
215–240. h ps://doi.o g/10.3897/
phy okeys.263.165364
Phy oKeys 263: 215–240 (2025)
DOI: 10.3897/phy okeys.263.165364
216
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
he e ogenei y, pa icula ly in s yle ypes, b ac mo phology, and pollen wall
s uc u e (Me xmülle e al. 1977; Nylinde and Ande be g 2015). Al hough
Me xmülle e al. (1977) p o ided a sys ema ic o e iew based on palynolo-
gy, cy ology, and mo phology, Inuleae does no o m a dis inc monophyle ic
g oup, highligh ing he complexi y o i s classi ica ion (B eme 1987; Ande -
be g 1989; Kim and Jansen 1995).
Pollen mo phology has long con ibu ed o plan axonomy, suppo ing
species and genus iden i ica ion ac oss di e se plan g oups (E d man 1952;
La son and Sk a la 1962; Nowicke and Sk a la 1979; Fe guson 1985). In la ge
and axonomically complex amilies such as As e aceae, i also p o ides in-
sigh s in o in e gene ic ela ionships and e olu iona y ends (Sk a la e al.
1977, 2005; Zhao e al. 2000; Pe ei a Cou inho and Dinis 2007, 2009; Wo ley
e al. 2007; Osman 2011). Pollen mo phology is gene ally gene ically con-
se ed and shows limi ed a ia ion ac oss en i onmen al condi ions, which
enhances i s eliabili y as a axonomic cha ac e (Za ei and Za e 2005;
Blackmo e 2007; Kadluczka e al. 2022). Key palynological ai s, including
size, shape, ape u e ype, exine o namen a ion, and pe o a ion dimensions,
a e widely used o in e gene ic ela ionships and suppo axonomic classi-
ica ion (Heida ian e al. 2021; Li e al. 2021). Al hough pollen mo phology
ends o be conse ed wi hin gene a o As e aceae, sub le ai di e ences
can s ill assis in dis inguishing closely ela ed species (El-Ghazaly and An-
de be g 1995; Magen a e al. 2010; Ca ijo e al. 2013; Huang e al. 2017;
Cou inho e al. 2020; Ma ques e al. 2021).
Recen s udies on he palynology o he ibe Inuleae ha e made no able
p og ess. Inuleae pollen ypically exhibi s a ca ea e, echina e–mic ope o a e
exine (Leins 1971; Ande be g 2009), hough sub le in e speci ic a ia ions hold
phylogene ic signi icance. Fo example, Cya hocline has smalle g ains wi h
longe spines compa ed o Blumea (Peng e al. 2023). The h ee mo pho ypes
o Pulica ia we e iden i ied based on spine and sculp u ing ea u es (Cou inho
e al. 2011). P e ious wo k has emphasized he impo ance o exine mo phol-
ogy, pa icula ly spine shape and sculp u ing pa e ns, in species classi ica ion
and in p o iding consis en mo phological e idence o phylogene ic analyses
ac oss se e al gene a (Osman 2006; Pe ei a Cou inho and Dinis 2007; Za in e
al. 2010; Ka lıoğlu Kılıç e al. 2021). Howe e , despi e hese ad ances, palyno-
logical esea ch on Inuleae emains ela i ely spa se (Pe een 1999; Po npon-
g ung ueng e al. 2007; Bahadu e al. 2022), and he pollen cha ac e is ics o
many species a e s ill unclea .
Acco dingly, his s udy ocuses on 19 species o Inuleae o analyze pollen
mo phology and i s sys ema ic implica ions. De ailed pollen mo phological
da a o 11 species a e p esen ed he e o he i s ime. Species sampling
a ge ed lineages wi hin Inuleae conside ed in o ma i e o in e p e ing pol-
len cha ac e s, enabling lineage-awa e in e p e a ion among he sampled
axa. This s udy o ms he second pa o an ongoing in es iga ion in o pal-
ynological and e olu iona y pa e ns in As e aceae, ollowing ou wo k on
As e eae (Qu e al. 2025). The objec i es a e o (i) p o ide palynological
da a o Inuleae species using ligh mic oscopy (LM) and scanning elec on
mic oscopy (SEM); (ii) dis inguish species wi h simila mo phology based
on pollen ai s; and (iii) e alua e he ole o palynology in he axonomy o
his g oup.
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Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Ma e ials and me hods
Sampling
Nine een pollen samples we e selec ed om ouche specimens deposi ed in
he PE He ba ium a he Ins i u e o Bo any, Chinese Academy o Sciences. Sam-
pling ollowed a ibe-le el phylogene ic amewo k o co e majo lineages o
Inuleae. The selec ed axa include species om Blumea, Ca pesium, and all s ud-
ied gene a o he ibe (Table 1). Scien i ic names we e s anda dized acco ding
o Plan s o he Wo ld Online (h ps://powo.science.kew.o g/, accessed 7 July
2025). We e iewed p io palynological li e a u e o e i y whe he each species
had been examined p e iously, and his in o ma ion is summa ized in Table 1.
Pollen p epa a ion
Pollen samples we e ace olysed using s anda d me hods (E d man 1960) and
ixed in glyce ine jelly. P ocessing and obse a ion unde LM and SEM ollowed
s anda d p ocedu es (Wang e al. 1995). Pollen g ains we e obse ed and pho-
og aphed a a magni ica ion o ×600 unde LM (Leica DM 4000) and a an
accele a ion ol age o 30 kV unde SEM (Hi achi S-4800). P io o SEM analy-
sis, samples we e spu e -coa ed wi h pla inum o enhance image quali y and
ensu e conduc i i y. Desc ip ions o pollen mo phological ai s ollow he e -
minology sys ems o Hesse and Blackmo e (2013) and Halb i e e al. (2018).
Table 1. Lis o he ouche specimens in he PE He ba ium, Ins i u e o Bo any, Chinese Academy o Sciences.
Species Sub ibe (Fu
e al. 2016) Locali y Collec ion
Da e Collec o Specimen
ba codes
Palynological
eco d
Blumea balsami e a (L.) DC. Inulinae Guizhou, China 10 Ap . 1959 Qiannan Team PE 00569129 Peng e al. 2023
Blumea megacephala (Rande ia) C.T.Chang
& C.H.Yu
Inulinae Guangxi, China 10 Dec. 2015 Z. Y. Zhang e al. PE 02112569 Peng e al. 2023
Blumea lace a (Bu m. .) DC. Inulinae Guangxi, China 15 Ap . 1998 H. N. Qin e al. PE 01997400 Peng e al. 2023
Blumea is ulosa (Roxb.) Ku z Inulinae Guangdong, China 5 Ap . 1997 Shenzhen
Expedi ion Team
PE 01401511 Peng e al. 2023
Blumea lanceola ia (Roxb.) D uce Inulinae Guangxi, China 7 No . 2010 Y. S. Chen PE 02110949 Fi s epo
Blumea o mosana Ki am. Inulinae Jiangxi, China 7 Oc . 1980 Sou he n
G assland Team
PE 01776724 Fi s epo
Ca pesium szechuanense F.H.Chen & C.M.Hu Inulinae Sichuan, China 8 Aug. 2007 Y. S. Chen PE 01670507 Fi s epo
Ca pesium is e Maxim. Inulinae Tochigi, Japan 28 Aug. 1988 M. Fu use PE 01292635 Fi s epo
Ca pesium co da um F.H.Chen & C.M.Hu Inulinae Sichuan, China 13 Jul. 2005 D.E.Bou o d e al. PE 01882433 Fi s epo
Ca pesium ce nuum L. Inulinae Henan, China Aug. 2009 Yun ai Moun ain
collec ion Team
PE 02015903 Za in e al. 2010
Ca pesium longi olium F.H.Chen & C.M.Hu Inulinae Sichuan, China 5 Sep. 2010 Gulin Expedi ion
Team
PE 01864636 Fi s epo
Inula japonica Thunb. Inulinae Shaanxi, China 18 Jul. 1953 K. J. Fu PE 00571428 Fi s epo
Ka elinia caspia (Pall.) Less. Plucheinae Gansu, China 12 Aug. 1964 -PE 01577784 Lu e al. 2018
Lagge a c ispa a (Vahl) Heppe & J.R.I.Wood Plucheinae Guizhou, China 2 May 2003 G. F. Wang PE 01688665 Fi s epo
Lagge a ala a (D. Don) Sch.Bip. ex Oli . Plucheinae Guizhou, China 7 Ap . 2004 F. C. Wang PE 01717274 Meo and Khan 2009
Pen anema indicum a . hypoleucum (Hand.-
Mazz.) Y.Ling
Inulinae Guizhou, China 15 Ma . 1960 Guizhou Team PE 01711140 Fi s epo
Pen anema ce nuum (Dalzell) Y.Ling Inulinae Yunnan, China -A. Hen y PE 01711084 Fi s epo
P e ocaulon edolens (Willd.) Fe n.-Vill. Plucheinae Queensland, Aus alia 1 Dec. 2012 K. R. McDonald PE 02110665 Fi s epo
Pulica ia dysen e ica (L.) Be nh. Inulinae Is ia, Slo enia 7 Sep. 2009 V. Mikolas e al. PE 02012570 Cou inho e al. 2011
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Da a acquisi ion
As shown in Fig. 1, pollen mo phological ai s measu ed unde LM included
P: pola leng h in equa o ial iew; E: equa o ial wid h in equa o ial iew; P/E; T:
exine hickness in pola iew; L: pollen leng h in pola iew; and T/L. Each ai
was measu ed o 20 pollen g ains pe species. The exine o namen a ion ai s
measu ed unde SEM included D: diame e o spine base; H: spine heigh ; D/H;
and Ss: spine spacing. Fo hese ou ai s, measu emen s we e aken on i e
pollen g ains pe ai , wi h ou andomly selec ed egions pe pollen g ain,
esul ing in 20 measu emen s pe ai (W ońska-Pila ek e al. 2015; Lu e al.
2022). Pollen shape ypes we e de e mined based on P/E a ios, ollowing he
de ini ions o E d man (1969) and Wang e al. (1995). G ains we e ca ego ized
as pe p ola e (P/E > 2), p ola e (1.32 < P/E ≤ 2), subp ola e (1.14 < P/E ≤ 1.32),
o sphe ical (0.88 < P/E ≤ 1.14). Desc ip i e mo phological e minology ollows
Pun e al. (2007). Mean (M) and s anda d de ia ion (SD) alues o 10 pollen
ai s we e calcula ed ac oss 19 species (Table 2, Suppl. ma e ial 1).
Da a analysis
Boxplo s o he 10 pollen ai s we e gene a ed using O iginP o 2025. To
elimina e dimensional e ec s and imp o e compa abili y, ai da a we e
s anda dized using Z-sco es (And ade 2021). P incipal componen analysis
Table 2. Pollen mo phological ai s o 19 selec ed species (Ss: spine spacing; D: diame e o spine base; H: spine heigh ;
P: pola leng h in equa o ial iew; E: equa o ial wid h in equa o ial iew; T: exine hickness in pola iew; L: pollen leng h
in pola iew).
Species Ss (μm) D (μm) H (μm) D/H P (μm) E (μm) P/E T (μm) L (μm) T/L
Blumea balsami e a (L.) DC. 4.79±0.23 3.39±0.12 3.58±0.17 0.95±0.03 28.82±1.48 26.86±1.12 1.07±0.04 4.27±0.27 28.04±1.29 0.15±0.01
Blumea megacephala (Rande ia)
C.T.Chang & C.H.Yu
6.01±0.55 3.69±0.36 3.95±0.36 0.93±0.04 26.68±1.66 24.76±1.21 1.08±0.04 4.10±0.30 27.50±1.29 0.15±0.01
Blumea lace a (Bu m. .) DC. 4.80±0.43 3.00±0.17 3.98±0.23 0.75±0.04 25.70±1.48 25.54±0.97 1.01±0.05 4.09±0.26 27.07±1.57 0.15±0.01
Blumea is ulosa (Roxb.) Ku z 4.92±0.42 3.31±0.34 3.86±0.40 0.86±0.06 29.94±1.67 27.58±1.58 1.09±0.03 4.05±0.18 30.20±1.10 0.13±0.00
Blumea lanceola ia (Roxb.) D uce 5.41±0.39 3.13±0.27 3.61±0.24 0.87±0.04 27.72±0.67 25.73±0.64 1.08±0.02 3.96±0.23 28.23±1.60 0.14±0.01
Blumea o mosana Ki am. 5.69±0.24 3.26±0.19 4.09±0.24 0.80±0.03 32.90±1.66 29.79±1.50 1.10±0.02 4.14±0.13 30.35±1.37 0.14±0.01
Ca pesium szechuanense F.H.Chen
& C.M.Hu
5.23±0.44 2.96±0.22 4.34±0.33 0.68±0.03 31.43±0.97 28.86±0.90 1.09±0.02 4.53±0.19 31.55±1.41 0.14±0.00
Ca pesium is e Maxim. 5.08±0.27 2.96±0.31 3.74±0.38 0.79±0.04 31.60±0.83 29.12±0.70 1.09±0.02 4.06±0.21 30.16±1.55 0.13±0.00
Ca pesium co da um F.H.Chen &
C.M.Hu
5.29±0.23 3.16±0.16 4.11±0.22 0.77±0.04 34.34±1.00 32.16±0.97 1.07±0.01 4.66±0.12 33.49±0.84 0.14±0.00
Ca pesium ce nuum L. 5.70±0.32 3.47±0.13 4.32±0.24 0.80±0.04 31.73±0.82 28.82±0.66 1.10±0.02 4.56±0.17 30.95±1.13 0.15±0.00
Ca pesium longi olium F.H.Chen &
C.M.Hu
6.34±0.51 3.75±0.35 5.17±0.55 0.73±0.04 35.06±1.41 32.42±1.70 1.08±0.03 5.12±0.18 32.98±1.20 0.16±0.01
Inula japonica Thunb. 5.06±0.33 2.90±0.24 3.51±0.27 0.83±0.03 27.51±0.74 26.23±0.91 1.05±0.02 3.86±0.13 27.06±1.04 0.14±0.00
Ka elinia caspia (Pall.) Less. 5.62±0.23 3.28±0.13 3.79±0.17 0.87±0.03 31.28±0.81 27.69±0.90 1.13±0.02 4.33±0.21 29.65±1.19 0.15±0.00
Lagge a c ispa a (Vahl) Heppe &
J.R.I.Wood
5.76±0.17 3.27±0.19 3.83±0.14 0.85±0.03 27.19±1.20 25.51±1.15 1.07±0.02 3.94±0.21 27.97±0.82 0.14±0.01
Lagge a ala a (D. Don) Sch.Bip. ex
Oli .
4.65±0.26 2.75±0.16 3.22±0.13 0.85±0.03 27.19±1.42 24.51±1.33 1.11±0.03 3.75±0.22 26.62±0.93 0.14±0.01
Pen anema indicum a . hypoleucum
(Hand.-Mazz.) Y.Ling
4.38±0.27 2.52±0.18 2.91±0.24 0.87±0.02 23.51±0.91 22.39±0.75 1.05±0.03 3.18±0.19 23.26±0.73 0.14±0.01
Pen anema ce nuum (Dalzell) Y.Ling 4.51±0.18 2.60±0.10 2.96±0.14 0.88±0.03 22.64±0.92 21.36±0.82 1.06±0.03 3.20±0.14 23.05±1.06 0.14±0.01
P e ocaulon edolens (Willd.) Fe n.-Vill. 4.42±0.21 2.42±0.10 2.69±0.11 0.90±0.02 22.77±1.56 22.00±1.52 1.04±0.02 3.06±0.12 22.67±1.31 0.14±0.01
Pulica ia dysen e ica (L.) Be nh. 4.22±0.29 2.56±0.16 3.32±0.13 0.77±0.05 23.85±1.22 22.29±1.18 1.07±0.02 3.06±0.18 23.69±1.68 0.13±0.01
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
(PCA) was pe o med wi h he p comp unc ion in R (R Co e Team. 2019) o
educe dimensionali y, iden i y ai co ela ions, and de e mine he a iables
con ibu ing mos o o al a iance. PCA p ojec ions we e isualized using
ggplo 2. One-way analysis o a iance (ANOVA) and Pea son’s co ela ion
analysis we e ca ied ou in SPSS 26.0 (IBM Co p., A monk, NY) o es in-
e speci ic di e ences in ai means and gene a e a co ela ion ma ix. Hi-
e a chical clus e analysis (HCA) was conduc ed in O iginP o 2025 based
on 10 quan i a i e palynological ai s (Ss, D, H, D/H, P, E, P/E, T, L, and T/L),
wi h Euclidean dis ances calcula ed and clus e ing pe o med using Wa d’s
me hod (Ye e al. 2015).
Resul s
Pollen mo phological cha ac e is ics
De ailed pollen mo phological da a obse ed unde LM and SEM a e p esen ed
in Figs 2–6. Quan i a i e alues o 10 pollen ai s ac oss species a e sum-
ma ized in Table 2, wi h he mean ± s anda d de ia ion (M ± SD) epo ed o
each ai . Boxplo s in Fig. 7 illus a e he dis ibu ion pa e ns o hese da a,
highligh ing he in e qua ile ange (25%–75%).
Figu e 1. G aphical illus a ion o measu ed pollen mo phological ai s in Inuleae
(A. Inula japonica; B. Ka elinia caspia; C. Blumea is ulosa; D. Ca pesium ce nuum). The
scale ba in he LM and SEM o e iew ep esen s 10 µm.
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Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Figu e 2. LM mic og aphs o pollen g ains in equa o ial iew. A. Blumea balsami e a; B. B. megacephala; C. B. lace a;
D. B. is ulosa; E. B. lanceola ia; F. B. o mosana; G. Ca pesium szechuanense; H. C. is e; I. C. co da um; J. C. ce nuum;
K. C. longi olium; L. Inula japonica; M. Ka elinia caspia; N. Lagge a c ispa a; O. L. ala a; P. Pen anema indicum a . hypo-
leucum; Q. P. ce nuum; R. P e ocaulon edolens; S. Pulica ia dysen e ica. Scale ba s ep esen s 10 µm.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Figu e 3. LM mic og aphs o pollen g ains in pola iew. A. Blumea balsami e a; B. B. megacephala; C. B. lace a;
D. B. is ulosa; E. B. lanceola ia; F. B. o mosana; G. Ca pesium szechuanense; H. C. is e; I. C. co da um; J. C. ce nuum;
K. C. longi olium; L. Inula japonica; M. Ka elinia caspia; N. Lagge a c ispa a; O. L. ala a; P. Pen anema indicum a . hypo-
leucum; Q. P. ce nuum; R. P e ocaulon edolens; S. Pulica ia dysen e ica. The scale ba ep esen s 10 µm.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Figu e 4. SEM mic og aphs o pollen g ains. Fo each species, ou images a e a anged in a ow: 1. Equa o ial iew; 2. Equa o ial
de ail; 3. Pola iew; 4. Pola de ail. A1–A4. Blumea balsami e a; B1–B4. B. megacephala; C1–C4. B. lace a; D1–D4. B. is ulosa;
E1–E4. B. lanceola ia; F1–F4. B. o mosana. The scale ba s ep esen 10 µm in o e iews and 1 µm in de ails.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Figu e 5. SEM mic og aphs o pollen g ains. Fo each species, ou images a e a anged in a ow: 1. Equa o ial iew; 2. Equa o ial
de ail; 3. Pola iew; 4. Pola de ail. A1–A4. Ca pesium szechuanense; B1–B4. C. is e; C1–C4. C. co da um; D1–D4. C. ce nu-
um; E1–E4. C. longi olium; F1–F4. Inula japonica. The scale ba s ep esen 10 µm in o e iews and 1 µm in de ails.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
ai s, indica ing ha species wi h mo e elonga ed spines ended o ha e small-
e pollen g ains. The ma ix o ea u e co ela ions (Table 4) suppo s hese
obse a ions. Pulica ia dysen e ica, posi ioned a he ex eme nega i e ends o
bo h PC1 and PC2, p esen ed ma kedly small pollen g ains and dis inc o na-
men a ion ea u es, possibly ep esen ing an ou lie ela i e o he main clus e .
O e all, he PCA indica ed ha pollen size ai s accoun o he majo i y o
obse ed a ia ion, while exine o namen a ion p o ides complemen a y dimen-
sions o in e speci ic di e en ia ion.
The palynological g oups o he species we e e alua ed using hie a chical
clus e analysis based on hei mo phological ai s. The analysis sepa a ed
he 19 Inuleae species in o wo majo g oups, G oup A and G oup B, wi h G oup
A u he di iding in o subg oups A1 and A2 (Fig. 9). The Euclidean dis ances
be ween G oup A and G oup B we e 10.31 and 3.01, espec i ely. G oup A in-
cluded 15 species, wi h subg oup A1 consis ing o 7 species, such as Blumea
balsami e a, B. megacephala, and Inula japonica, while subg oup A2 comp ised
8 species, including all 5 Ca pesium species, along wi h B. is ulosa, B. o mo-
sana, and Ka elinia caspia. G oup B consis ed o 4 species: Pen anema indicum
a . hypoleucum, P. ce nuum, P e ocaulon edolens, and Pulica ia dysen e ica.
Figu e 8. P incipal Componen s Analysis g aph showing he con ibu ion o he en a ibu es o explain a ia ion in pollen
g ains o he s udied Inuleae species; P. Pola leng h in equa o ial iew; E. Equa o ial wid h in equa o ial iew, P/E, T. Exine
hickness in pola iew, L. Pollen leng h in pola iew, T/L, D. Diame e o spine base, H. Spine heigh , D/H, Ss. Spine spacing.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Discussion
This s udy documen ed subs an ial in e -indi idual a ia ion in pollen mo phology
ac oss 19 Inuleae species, pa icula ly in g ain size and exine o namen a ion. All
species exhibi ed sphe ical pollen g ains wi h icolpo a e ape u es, and he ex-
ine su aces we e echina e. Va ia ions in spine mo phology p o ided measu able
di e ences be ween species, consis en wi h p e ious s udies on As e aceae (Sk-
a la e al. 1977; Osman 2006; Pe ei a Cou inho and Dinis 2007; Cou inho e al.
2011; Peng e al. 2023). These ai s con ibu e meaning ully o species delimi a-
ion and lay a mo phological ounda ion o u u e axonomic e inemen s wi hin
he ibe (Bahadu e al. 2022; Huang e al. 2023; Lin e al. 2023; Qu e al. 2025).
A compa a i e e iew was conduc ed o e alua e he consis ency o mo -
phological ai s ac oss gene a. Among he Blumea species—B. balsami e a,
B. megacephala, B. lace a, and B. is ulosa—we obse ed icolpo a e pollen
wi h echina e o namen a ion, consis en wi h he desc ip ions in Peng e al.
(2023). Ou measu emen s o P and E we e gene ally la ge han hose epo -
ed in hei s udy, al hough he P/E a ios we e simila . Since hei s udy lacked
illus a ions, hese esul s should be u he alida ed. The pollen mo phology
o Lagge a c ispa a, o which da a a e epo ed o he i s ime, showed sub le
di e ences when compa ed o L. ala a, as epo ed by Meo and Khan (2009).
Mino a ia ions in P and E we e no ed, likely e lec ing gene ic di e si y, en i-
onmen al adap a ion, o me hodological di e ences in pollen p ocessing, as
p e iously sugges ed (Mo e al. 1997; Zhang and Qian 2011; Lu e al. 2022). The
pollen ai s o Inula japonica con o m o he mo phological ange es ablished
Figu e 9. Clus e diag am (Wa d’s me hod) o 19 Inuleae species based on en quan i a i e pollen ai s.
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
by Ka lıoğlu Kılıç e al. (2021) o he genus Inula. Simila ly, Pulica ia dysen-
e ica shows pa e ns consis en wi h obse a ions by Cou inho e al. (2011),
suppo ing ai s abili y. The mo phology o Ka elinia caspia, he only species
in i s mono ypic genus, co esponds o da a epo ed by Lu e al. (2018). These
consis encies suppo he eliabili y o ou measu emen s. In he genus Ca pe-
sium, in addi ion o C. ce nuum, whose pollen mo phology was s udied by Za in
e al. (2010), we p o ide he i s desc ip ions o C. szechuanense, C. is e,
C. co da um, and C. longi olium, con ibu ing o he unde s anding o pollen
mo phology wi hin he genus. Addi ionally, his s udy es ablishes he i s pol-
len mo phological da ase o he genus Pen anema and ex ends p e ious wo k
on P e ocaulon (Co êa e al. 2008) by o e ing quan i a i e da a on P. edolens,
ansi ioning om quali a i e o quan i a i e documen a ion.
The gene a Blumea DC. and Ca pesium L. a e majo membe s o he sub-
ibe Inulinae wi hin Inuleae. Blumea is he la ges genus in he ibe (Ande be g
1991), p edominan ly consis ing o he bs o sh ubs, wi h he highes di e si y in
he opics o he Old Wo ld (Chen and Ande be g 2011a; Po npong ung ueng e
al. 2016). Many species ha e no able economic and ecological alue, wi h o e
hal possessing medicinal o e hnobo anical uses (Jia and Li 2005; Zhang e al.
2019). Howe e , axonomic con usion pe sis s due o limi ed mo phological s ud-
ies (Gagnepain 1920; Po npong ung ueng e al. 2007, 2016). Ca pesium, wi h ap-
p oxima ely 20 species (Zhang e al. 2015), is dis ibu ed in Asia and Eu ope, pa -
icula ly in moun ainous egions o Sou hwes China, whe e se e al species a e
endemic (Chen and Ande be g 2011b). The genus is also alued o i s medicinal
applica ions in adi ional he bal medicine (Kim e al. 1997; Moon 2007; Chung
e al. 2008; Moon and Zee 2011), bu i s palynology emains unde s udied (Za in
e al. 2010; Peng e al. 2023). Compa a i e analysis e eals dis inc di e ences
in pollen mo phology be ween he wo gene a. The maximum pola leng h (P) in
Blumea eaches 32.90 µm and equa o ial wid h (E) 29.79 µm, while in Ca pesium,
P is 35.06 µm and E is 32.42 µm. Pollen leng h (L) in Blumea anges om 27.07
o 30.35 µm, whe eas in Ca pesium i anges om 30.16 o 33.49 µm. These mea-
su emen s indica e ha Blumea pollen g ains a e gene ally smalle . Di e ences in
exine o namen a ion a e use ul o species iden i ica ion, hough u he s udy o
addi ional species is necessa y o con i ma ion. The spine base diame e (D) in
Blumea anges om 3.00 o 3.69 µm, wi h spine heigh (H) om 3.58 o 4.09 µm,
yielding a D/H a io o 0.75 o 0.95. In Ca pesium, while D (2.96 o 3.75 µm) is
simila , H is highe (3.74 o 5.17 µm), esul ing in a lowe D/H a io (0.68 o 0.80)
and mo e slende spines. Fu he mo e, spine spacing (Ss) in Blumea is na owe
(4.79 o 6.01 µm) compa ed o Ca pesium (5.08 o 6.34 µm), e lec ing a dense
o namen a ion pa e n. These pollen ai s p o ide mo phological e idence ha
may aid in dis inguishing he wo gene a, al hough u he s udy is needed o con-
i m hei diagnos ic alue in gene ic delimi a ion wi hin Inuleae.
PCA highligh ed pollen size and exine o namen a ion as key con ibu o s o
mo phological di e en ia ion among species (Wang e al. 2009; Zhang e al. 2017;
Maciejewska-Ru kowska e al. 2021; Ja dine e al. 2022). PC1 (67.39% a iance)
mainly e lec s size- ela ed ai s, while PC2 (13.67%) cap u es a ia ion in exine
o namen a ion. Species on he posi i e PC1 axis, such as C. longi olium and C. ce -
nuum, exhibi la ge pollen g ains. In con as , species on he nega i e axis, such
as Pulica ia dysen e ica and Pen anema ce nuum, show smalle pollen. PC2 u -
he sepa a es species by exine o namen a ion, especially D/H and T/L a ios. Fo
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
ins ance, B. megacephala and B. balsami e a ha e high D/H and T/L a ios, which
may enhance pollen igidi y unde a id o s ess ul condi ions (Wodehouse 1935;
Zhang and Zhou 2016). Con e sely, C. szechuanense and C. is e occupy nega i e
PC2 posi ions, wi h dis inc o namen a ion pa e ns possibly e lec ing en i on-
men al adap a ions (Tanaka e al. 2004; Ejsmond e al. 2011; Ďu išo á e al. 2023).
Acco ding o Fu e al. (2016), he Inuleae ibe is di ided in o wo sub ibes,
Inulinae and Plucheinae. The 19 species in his s udy belong o hese wo sub-
ibes (Table 1). To explo e he ole o pollen ai s in species di e en ia ion, we
pe o med hie a chical clus e analysis. The HCA esul s di ided he 19 species
in o wo main g oups (G oup A and G oup B), wi h G oup A u he spli in o
A1 and A2 subg oups. This di ision p ima ily aligns wi h a pollen size g adi-
en , as s ongly indica ed by PC1 (Fig. 8), bu also e eals in iguing pa e ns
when compa ed o phylogene ic classi ica ions. G oup A1 includes species
om Blumea, Lagge a, and Inula. Nylinde and Ande be g (2015) no ed ha he
bounda ies be ween Blumea and Lagge a a e unclea , and some species show
high mo phological simila i y. Ou palynological da a p o ide quan i a i e sup-
po o his obse a ion, as hese gene a sha e in e media e alues in key ai s
like Ss and D/H a io (Table 2), which may explain hei clus e ing in he HCA.
G oup A2 includes all Ca pesium species, along wi h B. is ulosa, B. o mosana,
and Ka elinia caspia (Plucheinae). The clus e ing o all i e Ca pesium species
sugges s s ong palynological consis ency wi hin he genus. The placemen o
K. caspia he e is incong uen wi h i s sub ibal classi ica ion bu is obus ly sup-
po ed by sha ed ai s like la ge pollen size and wide spine spacing (Table 2),
highligh ing he complex ole o pollen e olu ion in axonomy. G oup B consis s
o ou species. The wo Pen anema species a e clus e ed oge he , while he
P e ocaulon and Pulica ia species a e in sepa a e b anches. These species ha e
smalle pollen sizes, wi h P alues anging om 22.64 o 23.85 µm. PCA analy-
sis suppo s his, wi h G oup B species p ima ily loca ed in he nega i e egion
o he PC1 axis (Fig. 8). The igh clus e ing o he wo Pen anema species, in
pa icula , unde sco es he u ili y o pollen mo phology o delimi ing closely e-
la ed species. These esul s sugges ha pollen size is a key ea u e o species
di e en ia ion (Lu e al. 2009; Chung e al. 2010; Usma e al. 2022). Taken o-
ge he , he HCA esul s a e la gely consis en wi h he g oupings sugges ed by
PCA, con i ming he ole o pollen ai s in species di e en ia ion. Howe e , hey
do no ully align wi h molecula phylogene ic g oups (Lin e al. 2023), and he
incong uence in plan sys ema ics may need in eg a i e axonomic app oaches
(Kea ing e al. 2023). PCA iden i ied pollen size and exine o namen a ion as he
mos in luen ial ai s, while HCA e ealed species g oupings based on o e all
pollen mo phological simila i y. Toge he , hey con i m he signi ican alue o
pollen mo phological da a o he classi ica ion wi hin Inuleae.
Quan i a i e pollen mo phological da a om 19 Inuleae species p o ide alu-
able insigh s in o he sys ema ic palynology o As e aceae. In his s udy, one
specimen pe species was analyzed, a common p ac ice in palynological esea ch
(Bahadu e al. 2022; Lu e al. 2022; Peng e al. 2023). While his app oach acili-
a es in e speci ic compa isons, u u e s udies could expand sampling o be e
assess he ange and consis ency o pollen ai s, including ploidy coun ing and
he e alua ion o de ec i e o s e ile pollen. To cap u e po en ial nonlinea a ia-
ion, dimensionali y educ ion echniques such as UMAP may complemen PCA
(McInnes e al. 2018; Bech e al. 2019; E b e al. 2024). Highe - esolu ion imag-
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Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
ing me hods, such as ansmission elec on mic oscopy (TEM) combined wi h
SEM, could esol e ine-scale exine s uc u es (Jia e al. 2017; Gaba aye a e al.
2024). Combining mo phological, genomic, and ansc ip omic da a may e eal
he gene ic basis o pollen a ia ion and i s e olu iona y signi icance (Kea ing e
al. 2023; Qu e al. 2025). These app oaches could e ine species delimi a ion and
cla i y pollen e olu ion wi hin a b oade phylogene ic con ex .
Conclusion
This s udy documen ed a ia ion in pollen mo phology among 19 Inuleae
species, ocusing on g ain size, shape, and exine o namen a ion. These ai s
p o ed use ul in dis inguishing species and con ibu ed o axonomic classi i-
ca ion. While HCA and PCA e ined species clus e ing based on pollen ai s,
he axonomic ela ionships among species canno be ully cla i ied by pollen
mo phology alone. These esul s p o ide a ounda ion o u u e esea ch on
he ole o pollen mo phology in species di e en ia ion wi hin Inuleae.
Acknowledgemen s
The au ho s hank D . Xiuping Xu (Ins i u e o Bo any, Chinese Academy o
Sciences) o expe guidance in SEM and he anonymous e iewe s o hei
in aluable commen s, which g ea ly imp o ed he quali y o his manusc ip .
Addi ional in o ma ion
Con lic o in e es
The au ho s ha e decla ed ha no compe ing in e es s exis .
E hical s a emen
No e hical s a emen was epo ed.
Use o AI
No use o AI was epo ed.
Funding
This s udy was suppo ed by he Na ional Na u al Science Founda ion o China (Nos.
32000158, 42077423), he Na ional Science & Technology Fundamen al Resou ces In-
es iga ion P og am o China (No. 2021XJKK0702), he Founda ion o Sus ainable De-
elopmen Resea ch Cen e o Resou ces and En i onmen o Wes e n Sichuan, Sichuan
No mal Uni e si y (No. 2020CXZYHJZX03), he Key Labo a o y o Chemis y in E hnic
Medicinal Resou ces (Yunnan Minzu Uni e si y), he S a e E hnic A ai s Commission &
Minis y o Educa ion (No. MZY2301), and he Key Resea ch and De elopmen P og am
o Leshan Science and Technology Plan (No. 24ZDYF0099).
Au ho con ibu ions
TQ: concep ualiza ion, w i ing—o iginal d a ; XC: so wa e, o mal analysis; XZ: o mal
analysis, da a cu a ion; YZ: o mal analysis; YS: da a cu a ion; HS: da a cu a ion; BZ:
da a cu a ion; GX: esou ces, w i ing— e iew and edi ing; ZF: concep ualiza ion, w i -
ing— e iew and edi ing. All au ho s ead and app o ed he inal manusc ip .
235
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Au ho ORCIDs
Tianmeng Qu h ps://o cid.o g/0009-0008-0185-5306
Xinyu Chen h ps://o cid.o g/0009-0008-6347-2490
Xinyi Zheng h ps://o cid.o g/0009-0003-2300-5525
Yan u Zhang h ps://o cid.o g/0009-0009-0450-2001
Yizhen Shao h ps://o cid.o g/0000-0002-8865-3959
Hongze Sun h ps://o cid.o g/0009-0000-5831-9979
Bing Zhang h ps://o cid.o g/0009-0006-6019-0629
Gan Xie h ps://o cid.o g/0000-0002-8265-1565
Zhixi Fu h ps://o cid.o g/0000-0002-2789-6287
Da a a ailabili y
All o he da a ha suppo he indings o his s udy a e a ailable in he main ex o
Supplemen a y In o ma ion.
Re e ences
Ande be g AA (1989) Phylogeny and eclassi ica ion o he ibe Inuleae (As e aceae).
Canadian Jou nal o Bo any 67: 2277–2296. h ps://doi.o g/10.1139/b89-292
Ande be g AA (1991) Taxonomy and phylogeny o he ibe Inuleae (As e aceae). Plan
Sys ema ics and E olu ion 176: 75–123. h ps://doi.o g/10.1007/BF00937947
Ande be g AA (2009) Inuleae. In: Funck VA, Susanna A, S uessy TF, Baye RJ (Eds)
Sys ema ics, E olu ion, and Biogeog aphy o Composi ae. She idan Books Inc, Ann
A bo , 667–680.
Ande be g AA, Eldenäs P (2007) Inuleae. In: Kade ei JW, Je ey C (Eds) The Families
and Gene a o Vascula Plan s Vol. 8. Flowe ing Plan s Eudico s: As e ales. Sp inge ,
Be lin, 374–375.
And ade C (2021) Z Sco es, s anda d sco es, and composi e es sco es ex-
plained. Indian Jou nal o Psychological Medicine 43: 555–557. h ps://doi.
o g/10.1177/02537176211046525
Bahadu S, Taj S, Long WQ, Ahmad M (2022) Pollen mo phology and i s implica ion
in he axonomy o some selec ed ibes o he As e aceae o Hainan Island Sou h
China. Bo anical Re iew 88: 271–298. h ps://doi.o g/10.1007/s12229-022-09277-3
Bech E, McInnes L, Healy J, Du e e CA, Kwok IWH, Ng LG, Ginhoux F, Newell EW (2019)
Dimensionali y educ ion o isualizing single-cell da a using UMAP. Na u e Bio ech-
nology 37: 38–44. h ps://doi.o g/10.1038/nb .4314
Blackmo e S (2007) Pollen and spo es: Mic oscopic keys o unde s anding he ea h’s
biodi e si y. Plan Sys ema ics and E olu ion 263: 3–12. h ps://doi.o g/10.1007/
s00606-006-0464-3
B eme K (1987) T ibal in e ela ionships o he As e aceae. Cladis ics: The In-
e na ional Jou nal o he Willi Hennig Socie y 3: 210–253. h ps://doi.
o g/10.1111/j.1096-0031.1987. b00509.x
Ca ijo TT, Ga bin ML, Picanço Lei e W, Mendonça CBF, Es e es RL, Gonçal es-Es e es V
(2013) Pollen mo phology o some ela ed gene a o Ve nonieae (As e aceae) and i s
axonomic signi icance. Plan Sys ema ics and E olu ion 299: 1275–1283. h ps://
doi.o g/10.1007/s00606-013-0795-9
Chen YS, Ande be g AA (2011a) Blumea DC. In: Wu ZY, Ra en PH, Hong DY (Eds) Flo a
o China, Vol. 20–21. Science P ess, Beijing; Missou i Bo anical Ga den P ess, S .
Louis, 829 pp.
236
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Chen YS, Ande be g AA (2011b) Ca pesium L. In: Wu ZY, Ra en PH, Hong DY (Eds) Flo a
o China, Vol. 20–21. Science P ess, Beijing; Missou i Bo anical Ga den P ess, S .
Louis, 821 pp.
Chung I, Kim M, Moon H (2008) An iplasmodial ac i i y o sesqui e pene lac one om
Ca pesium osula um in mice. Pa asi ology Resea ch 103: 341–344. h ps://doi.
o g/10.1007/s00436-008-0977-5
Chung KS, Elisens WJ, Sk a la JJ (2010) Pollen mo phology and i s phylogene ic signi i-
cance in ibe Sanguiso beae (Rosaceae). Plan Sys ema ics and E olu ion 285(3–4):
139–148. h ps://doi.o g/10.1007/s00606-009-0262-9
Co êa MVG, Lima LFP, Baue mann SG (2008) Mo ologia polínica das espécies b asilei-
as de P e ocaulon Ell. (As e aceae). Pesquisas. Sé ie Bo ânica (59): 263–276.
Cou inho AP, Aguia CF, Bandei a DSD, Dinis AM (2011) Compa a i e pollen mo phol-
ogy o he Ibe ian species o Pulica ia (As e aceae, Inuleae, Inulinae) and i s axo-
nomic signi icance. Plan Sys ema ics and E olu ion 297: 171–183. h ps://doi.
o g/10.1007/s00606-011-0505-4
Cou inho AP, Sil ei a P, Pi a C, San os MJ, Sa ai a C, Pe pé uo NC (2020) Pollen mo phol-
ogy o Xan hium L. (s.l.) (As e aceae, As e oideae, Helian heae, Amb osiinae) in he
Ibe ian Peninsula – a palyno axonomic app oach o a poisonous, alle genic and in-
asi e genus. G ana 60(1): 35–56. h ps://doi.o g/10.1080/00173134.2020.1737729
Ďu išo á Ľ, Ďú ano á H, Kšiňan S, E ns D, Šebes a M, Ži niak Ču ná V, Eliáš P, Qian
Y, S aka V, Feng H, Tomo ičo á L, Ko lá o á N, K a ošo á G, Kolenčík M (2023)
Explo ing he impac o me al-based nano e ilize s: A case s udy on sun lowe pol-
len mo phology and yield in ield condi ions. Ag onomy (Basel) 13(12): 2922. h ps://
doi.o g/10.3390/ag onomy13122922
Ejsmond MJ, W ońska-Pila ek D, Ejsmond A, D agosz-Kluska D, Ka pińska-Kołaczek
M, Kołaczek P, Kozłowski J (2011) Does clima e a ec pollen mo phology? Op imal
size and shape o pollen g ains unde a ious desicca ion in ensi y. Ecosphe e 2(10):
1–15. h ps://doi.o g/10.1890/ES11-00147.1
El-Ghazaly G, Ande be g AA (1995) Pollen mo phology o Phagnalon and Aliella (As e -
aceae, Gnaphalieae) and i s axonomical implica ions. G ana 34(2): 89–99. h ps://
doi.o g/10.1080/00173139509429999
E b S, G a E, Zede Y, Lione i S, Be ne A, Clo B, Liebe he G, Tummon F, Wullschlege
P, C ouzy B (2024) Real- ime pollen iden i ica ion using holog aphic imaging and lu-
o escence measu emen s. A mosphe ic Measu emen Techniques 17(2): 441–451.
h ps://doi.o g/10.5194/am -17-441-2024
E d man G (1952) Pollen mo phology and plan axonomy: angiospe ms. Almq is &
Wiksell, S ockholm. h ps://doi.o g/10.1080/11035895209453507
E d man G (1960) The ace olysis me hod, a e ised desc ip ion. S ensk Bo anisk Tid-
sk i 54: 561–564.
E d man G (1969) Handbook o palynology, mo phology, axonomy, ecology. An in o-
duc ion o he s udy o pollen g ains and spo es. Ha ne Pub, New Yo k.
Fe guson IK (1985) The ole o pollen mo phology in plan sys ema ics. Anales de la
Asociación de Palinólogos de Lengua Española 2: 5–18.
Fu ZX, Jiao BH, Nie B, Zhang GJ, Gao TG (2016) A comp ehensi e gene ic-le el phylogeny
o he sun lowe amily: Implica ions o he sys ema ics o Chinese As e aceae. Jou -
nal o Sys ema ics and E olu ion 54(4): 416–437. h ps://doi.o g/10.1111/jse.12216
Gaba aye a NI, B i ski DA, G igo je a VV (2024) Pollen wall de elopmen in Impa iens
glanduli e a: Exine subs uc u e and unde lying mechanisms. P o oplasma 261:
111–124. h ps://doi.o g/10.1007/s00709-023-01887-x
237
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Gagnepain MF (1920) Un gen e nou eau de Composées, Blumeopsis. Bulle in du
Muséum Na ional d’His oi e Na u elle 26: 75–76.
Halb i e H, Sil ia U, G ímsson F, Webe M, Ze e R, Hesse M, Buchne R, S oj ka M,
F osch-Radi o A (2018) Illus a ed Pollen Te minology. Sp inge , Cham, Swi ze land,
483 pp. h ps://doi.o g/10.1007/978-3-319-71365-6
Heida ian M, Masoumi SM, Ami i S (2021) Palynological s udy on selec ed species om
Hyacin haceae wi h ocus on axonomical implica ions in I an. Palynology 46(1):
1–16. h ps://doi.o g/10.1080/01916122.2021.1952329
Hesse M, Blackmo e S (2013) P e ace o he special ocus manusc ip s. Plan Sys ema -
ics and E olu ion 299: 1011–1012. h ps://doi.o g/10.1007/s00606-013-0811-0
Huang Y, An YM, Meng SY, Guo YP, Rao GY (2017) Taxonomic s a us and phylogene ic
posi ion o Phaeos igma in he sub ibe A emisiinae (As e aceae). Jou nal o Sys-
ema ics and E olu ion 55(5): 426–436. h ps://doi.o g/10.1111/jse.12257
Huang XK, Wu R, Xiong Z, Ma ZH (2023) Pollen mo phology o Cle odend um L. (Lamia-
ceae) om China and i s sys ema ic implica ions. Phy oKeys 235: 53–68. h ps://doi.
o g/10.3897/phy okeys.235.111516
Ja dine PE, Palazzesi L, Telle ía MC, Ba eda VD (2022) Why does pollen mo phology
a y? E olu iona y dynamics and mo phospace occupa ion in he la ges angiospe m
o de (As e ales). The New Phy ologis 234(3): 1075–1087. h ps://doi.o g/10.1111/
nph.18024
Jia M, Li X (2005) Chinese na ional pha macology, 1s ed. Chinese Medical Science
P ess, Beijing.
Jia PF, Li HJ, Yang WC (2017) T ansmission elec on mic oscopy (TEM) o s udy his-
ology o pollen and pollen ubes. In: Schmid A (Ed.) Plan Ge mline De elopmen ,
Vol. 1669. Humana P ess, New Yo k, 181–189. h ps://doi.o g/10.1007/978-1-4939-
7286-9_15
Kadluczka D, Sliwinska E, G zebelus E (2022) Combining genome size and pollen mo -
phology da a o s udy species ela ionships in he genus Daucus (Apiaceae). BMC
Plan Biology 22: 1–13. h ps://doi.o g/10.1186/s12870-022-03743-1
Ka lıoğlu Kılıç N, Yılmaz Dağde i en R, Paksoy MY, Tuncalı Yaman T (2021) Pollen mo -
phology o eigh endemic Inula L.(As e aceae) species in Tu key. Palynology 45(2):
235–244. h ps://doi.o g/10.1080/01916122.2020.1784306
Kea ing JN, Ga wood RJ, Sansom RS (2023) Phylogene ic cong uence, con lic and con-
silience be ween molecula and mo phological da a. BMC Ecology and E olu ion 23:
30. h ps://doi.o g/10.1186/s12862-023-02131-z
Kim KJ, Jansen RK (1995) NdhF sequence e olu ion and he majo clades in he sun-
lowe amily. P oceedings o he Na ional Academy o Sciences o he Uni ed S a es
o Ame ica 92(22): 10379–10383. h ps://doi.o g/10.1073/pnas.92.22.10379
Kim DK, Baek NI, Choi SU, Lee CO, Lee KR, Zee OP (1997) Fou new cy o oxic ge mac an-
olides om Ca pesium di a ica um. Jou nal o Na u al P oduc s 60(11): 1199–1202.
h ps://doi.o g/10.1021/np970157d
La son DA, Sk a la JJ (1962) An elec on mic oscope s udy o exine s a i ica ion and
ine s uc u e. Pollen e Spo es 4: 233–246.
Leins P (1971) Pollensys ema ische s udien an Inuleen, I: Ta chonan hineae, Pluchein-
ae, Inulinae, Buph halminae. Bo anische Jah büche ü Sys ema ik, P lanzenges-
chich e und P lanzengeog aphie 91: 91–146.
Li WW, Wang YN, Liu LQ, Niu YY, Zhao SR, Zhang SK, Wang YT, Liao K (2021) Pollen mo -
phology o selec ed ap ico (P unus) axa. Palynology 45(1): 95–102. h ps://doi.o g
/10.1080/01916122.2020.1737260
238
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Lin M, Qiu J, Xie K, Tan D (2023) Palynological ea u es and axonomic signi icance o
16 species o Gagea (Liliaceae) om Xinjiang, China. Phy oKeys 225: 53–68. h ps://
doi.o g/10.3897/phy okeys.225.101518
Lu L, F i sch PW, Wang H, Li HT, Li DZ, Chen JQ (2009) Pollen mo phology o Gaul he ia
L. and ela ed gene a o sub amily Vaccinioideae: Taxonomic and e olu iona y sig-
ni icance. Re iew o Palaeobo any and Palynology 154(1–4): 106–123. h ps://doi.
o g/10.1016/j. e palbo.2008.12.009
Lu KQ, Xie G, Li M, Li JF, T i edi A, Fe guson DK, Yao YF, Wang YF (2018) Da ase o pollen
mo phological ai s o 56 dominan species among dese ege a ion in he eas e n a id
cen al Asia. Da a in B ie 18: 1022–1046. h ps://doi.o g/10.1016/j.dib.2018.03.122
Lu LL, Jiao BH, Qin F, Xie G, Lu KQ, Li JF, Sun B, Li M, Fe guson DK, Gao TG, Yao YF, Wang
YF (2022) A emisia pollen da ase o explo ing he po en ial ecological indica o s in
deep ime. Ea h Sys em Science Da a 14(9): 3961–3995. h ps://doi.o g/10.5194/
essd-14-3961-2022
Maciejewska-Ru kowska I, Bocianowski J, W ońska-Pila ek D (2021) Co ec ion: Pollen
mo phology and a iabili y o Polish na i e species om genus Salix L. PLOS ONE 16:
e0252253. h ps://doi.o g/10.1371/jou nal.pone.0252253
Magen a MAG, Nunes ADD, Mendonça CBF, Gonçal es-Es e es V (2010) Palyno axon-
omy o B azilian Viguie a (As e aceae) species. Bole ín de La Sociedad A gen ina de
Bá anica 45: 285–299.
Ma ques D, Pico GMV, Nakajima JN, Dema eis M (2021) Pollen mo phology and i s
sys ema ic alue o sou he n Sou h Ame ican species o Lepidaploa (Ve nonieae:
As e aceae). Rod iguésia 72: 1–18. h ps://doi.o g/10.1590/2175-7860202172017
McInnes L, Healy J, Mel ille J (2018) Uni o m mani old app oxima ion and p ojec ion o
dimension educ ion. a Xi , 1802.03426. h ps://doi.o g/10.48550/a Xi .1802.03426
Meo AA, Khan MA (2009) Pollen mo phology o a e axa Lagge a ala a and i s ela ed
species Pluchea lanceola a o ibe Plucheeae (As e aceae). Pakis an Jou nal o Bo -
any 41: 1539–1544.
Me xmülle H, Leins P, Roessle H (1977) Inuleae – Sys ema ic e iew. In: Heywood VH,
Ha bo ne JB, Tu ne BL (Eds) The Biology and Chemis y o he Composi ae, Vol. 1.
Academic P ess, London, 577–602.
Mo RG, Bai XL, Ma YY, Cao R (1997) On he in aspeci ic a ia ions o pollen mo phology
and pollen geog aphy o a elic species – Helian hemum songa icum Sch enk. Xibei
Zhiwu Xuebao 17(4): 528–532.
Moon H (2007) An iplasmodial ac i i y o ineupa o olides A om Ca pesium osula um.
Pa asi ology Resea ch 100: 1147–1149. h ps://doi.o g/10.1007/s00436-006-0369-7
Moon H, Zee O (2011) Sesqui e pene lac ones om Ca pesium osula um wi h po en ial
cy o oxici y agains i e human cance cell lines. Human & Expe imen al Toxicology
30: 1083–1087. h ps://doi.o g/10.1177/0960327110386818
Nowicke JW, Sk a la JJ (1979) Pollen mo phology: The po en ial in luence in highe
o de sys ema ics. Annals o he Missou i Bo anical Ga den 66(4): 633–700. h ps://
doi.o g/10.2307/2398914
Nylinde S, Ande be g AA (2015) Phylogeny o he Inuleae (As e aceae) wi h special empha-
sis on he Inuleae‐Plucheinae. Taxon 64(1): 110–130. h ps://doi.o g/10.12705/641.22
Osman AK (2006) Con ibu ions o he pollen mo phology o he ibe Inuleae (sub amily
As e oideae‐Composi ae) in he lo a o Egyp . Feddes Repe o ium 117(3–4): 193–
206. h ps://doi.o g/10.1002/ ed .200511096
Osman AK (2011) Pollen mo phology o ibes Gnaphalieae, Helenieae, Plucheeae
and Senecioneae (sub amily As e oideae) o Composi ae om Egyp .
239
Phy oKeys 263: 215–240 (2025), DOI: 10.3897/phy okeys.263.165364
Tianmeng Qu e al.: Pollen mo phology and species di e en ia ion in Inuleae
Ame ican Jou nal o Plan Sciences 2(2): 120–133. h ps://doi.o g/10.4236/
ajps.2011.22014
Peng Y, Pu X, Yu Q, Zhou H, Huang T, Xu B, Gao X (2023) Compa a i e pollen mo phology
o selec ed species o Blumea DC. and Cya hocline Cass. and i s axonomic signi i-
cance. Plan s 12(16): 2909. h ps://doi.o g/10.3390/plan s12162909
Pe ei a Cou inho A, Dinis AM (2007) A con ibu ion o he ul as uc u al knowledge o
he pollen exine in sub ibe Inulinae (Inuleae, As e aceae). Plan Sys ema ics and
E olu ion 269: 159–170. h ps://doi.o g/10.1007/s00606-007-0585-3
Pe ei a Cou inho A, Dinis AM (2009) A ligh , scanning elec on and ansmission elec-
on mic oscopic s udy o pollen wall a chi ec u e in he sub ibe Gnaphaliinae
(Gnaphalieae, As e aceae). Plan Sys ema ics and E olu ion 283: 79–92. h ps://doi.
o g/10.1007/s00606-009-0216-2
Pe een A (1999) Con ibu ions o he pollen mo phology o he amily Composi ae.
Tu kish Jou nal o Biology = Tü k Biyoloji De gisi 23: 523–536. h ps://jou nals. ubi-
ak.go . /biology/ ol23/iss4/15/
Po npong ung ueng P, Bo chsenius F, Englund M, Ande be g AA, Gus a sson MHG
(2007) Phylogene ic ela ionships in Blumea (As e aceae: Inuleae) as e idenced by
molecula and mo phological da a. Plan Sys ema ics and E olu ion 269: 223–243.
h ps://doi.o g/10.1007/s00606-007-0581-7
Po npong ung ueng P, Gus a sson MHG, Bo chsenius F, Koyama H, Chan a ano hai P
(2016) Blumea (Composi ae: Inuleae) in con inen al Sou heas Asia. Kew Bulle in
71(1): 1. h ps://doi.o g/10.1007/s12225-016-9612-2
Pun W, Hoen PP, Blackmo e S, Nilsson S, Thomas LA (2007) Glossa y o pollen and
spo e e minology. Re iew o Palaeobo any and Palynology 143(1–2): 1–81. h ps://
doi.o g/10.1016/j. e palbo.2006.06.008
Qu TM, Xie G, Zheng XY, Chen XY, Zhang YR, Lu LL, Fu ZX (2025) Sys ema ic analysis
o some As e eae (As e aceae) species by in eg a ing pollen mo phology and mo-
lecula e idence. F on ie s in Plan Science 16: 1558995. h ps://doi.o g/10.3389/
pls.2025.1558995
R Co e Team (2019) R: A language and en i onmen o s a is ical compu ing. R Founda-
ion o S a is ical Compu ing. h ps://www. -p ojec .o g/
Sk a la JJ, Tu ne BL, Pa el VC, Tomb AS, Thanikaimoni G (1977) Pollen mo phology in
he Composi ae and in mo phologically ela ed amilies. In: Heywood VH, Ha bo ne
JB, Tu ne BL (Eds) The Biology and Chemis y o he Composi ae. Academic P ess,
London, 141–265.
Sk a la JJ, DeVo e ML, Chissoe WF (2005) Lopha e sculp u ing o Ve nonieae (Compos-
i ae) pollen. Re iew o Palaeobo any and Palynology 133(1–2): 51–68. h ps://doi.
o g/10.1016/j. e palbo.2004.09.001
Tanaka N, Ueha a K, Mu a a J (2004) Co ela ion be ween pollen mo phology and pol-
lina ion mechanisms in he Hyd ocha i aceae. Jou nal o Plan Resea ch 117: 265–
276. h ps://doi.o g/10.1007/s10265-004-0155-5
Usma A, Ahmad M, Za a M, Sul ana S, Ullah F, Saqib S, Ayaz A, Zaman W (2022) Paly-
nological s udy o weed lo a om Po oha Pla eau. Ag onomy (Basel) 12(10): 2500.
h ps://doi.o g/10.3390/ag onomy12102500
Wang FX, Qian NF, Zhang YL, Yang HQ (1995) Pollen mo phology o Chinese plan s, 2nd
ed. Science P ess, Beijing.
Wang H, Yu WB, Chen JQ, Blackmo e S (2009) Pollen mo phology in ela ion o lo al
ypes and pollina ion synd omes in Pedicula is (O obanchaceae). Plan Sys ema ics
and E olu ion 277: 153–162. h ps://doi.o g/10.1007/s00606-008-0112-1
