Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae
Pollen morphology of four species belonging to four genera of the tribe Cymbarieae and two species of Lindenbergia of the tribe Lindenbergieae (Orobanchaceae) was studied using light and scanning electron microscopy. Pollen grains in Lindenbergieae are 3-colporate (rarely 2-colporate), prolate, sp...
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Інститут ботаніки ім. М.Г. Холодного НАН України
2018
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| Цитувати: | Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae / Z.M. Tsymbalyuk, S.L. Mosyakin // Український ботанічний журнал. — 2018. — Т. 75, № 2. — С. 123-136. — Бібліогр.: 42 назв. — англ. |
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Tsymbalyuk, Z.M. Mosyakin, S.L. 2021-02-05T11:20:19Z 2021-02-05T11:20:19Z 2018 Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae / Z.M. Tsymbalyuk, S.L. Mosyakin // Український ботанічний журнал. — 2018. — Т. 75, № 2. — С. 123-136. — Бібліогр.: 42 назв. — англ. 0372-4123 DOI: https://doi.org/10.15407/ukrbotj75.02.123 https://nasplib.isofts.kiev.ua/handle/123456789/176539 Pollen morphology of four species belonging to four genera of the tribe Cymbarieae and two species of Lindenbergia of the tribe Lindenbergieae (Orobanchaceae) was studied using light and scanning electron microscopy. Pollen grains in Lindenbergieae are 3-colporate (rarely 2-colporate), prolate, spheroidal and oblate-spheroidal, small-sized, with reticulate exine sculpture. Pollen grains in Cymbarieae are 3-colpate, rarely 4-colpate, prolate, spheroidal and oblate-spheroidal, medium-sized. Exine sculpture in Cymbarieae is retipilate and rugulate-retipilate. Pollen characters of Cymbarieae and Lindenbergieae are compared with pollen patterns in Paulowniaceae and crown clades of Orobanchaceae. The earliest-branching clade of Orobanchaceae (Lindenbergieae) is palynomorphologically similar to Paulowniaceae (the clade sister to all Orobanchaceae) and to Wightia. These palynomorphological findings confirm the phylogenetic patterns recently revealed in basal Orobanchaceae and their closest relatives. It is concluded that the colporate (most probably 3-colporate) type of pollen grains could be ancestral in Orobanchaceae. Pollen diversity in crown clades of Orobanchaceae evolved on the base of a few pollen types and subtypes, which were peculiar to hypothetical ancestors of Orobanchaceae and are probably preserved in the extant taxa of Paulowniaceae and Lindenbergieae. З використанням світлової та сканувальної електрон- ної мікроскопії досліджено морфологію пилкових зерен чотирьох видів з чотирьох родів триби Cymbarieae та двох видів роду Lindenbergia триби Lindenbergieae (Orobanchaceae). Встановлено, що пилкові зерна триби Lindenbergieae 3-борозно-орові (зрідка 2-борозно-орові), еліпсоїдальні, сфероїдальні або сплющено-сфероїдальні за формою, дрібних розмірів, з сітчастою скульптурою екзини. Пилкові зерна триби Cymbarieae 3-борозні, зрідка 4-борозні, еліпсоїдальні, сфероїдальні або сплющено-сфероїдальні за формою, середніх або великих розмірів, з сітчасто-паличковою або зморшкувато-сітчасто-паличковою скульптурою екзини. Особливості пилкових зерен представників триб Cymbarieae і Lindenbergieae порівнюються з такими в Paulowniaceae і верхівкових кладах Orobanchaceae. Базальна клада Orobanchaceae (Lindenbergieae) за паліноморфологічними особливостями подібна до Paulowniaceae (сестринська клада до всіх Orobanchaceae) і Wightia. Паліноморфологічні висновки підтверджують філогенетичні закономірності, які виявлені у базальних Orobanchaceae та їхніх найближчих родичів. Зроблено висновок, що борозно-оровий (ймовірно, 3-борозно-оровий) тип пилкових зерен може бути предковим у родині Orobanchaceae. Різноманітність пилкових зерен у верхівкових кладах Orobanchaceae еволюціонувала на основі декількох типів і підтипів пилку, властивих гіпотетичним предкам Orobanchaceae; такі типи, ймовірно, збереглися в сучасних представників Paulowniaceae та Lindenbergieae. С помощью световой и сканирующей электронной микроскопии изучены пыльцевые зерна четырех видов из четырех родов трибы Cymbarieae и двух видов рода Lindenbergia трибы Lindenbergieae (Orobanchaceae). Установлено, что пыльцевые зерна трибы Lindenbergieae 3-бороздно-оровые (изредка 2-бороздно-оровые), эллипсоидальные, сфероидальные или сплющено-сфероидальные по форме, мелких размеров, с сетчатой скульптурой экзины. Пыльцевые зерна трибы Cymbarieae 3-бороздные, изредка 4-бороздные, эллипсоидальные, сфероидальные или сплющено-сфероидальные по форме, средних или больших размеров, с сетчато-палочковой или морщинисто-сетчасто-палочковой скульптурой экзины. Особенности пыльцевых зерен представителей триб Cymbarieae и Lindenbergieae сравниваются с таковыми у Paulowniaceae и терминальных клад Orobanchaceae. Базальная клада в семействе Orobanchaceae (Lindenbergieae) по палиноморфологическим особенностям сходна с Paulowniaceae (сестринская клада по отношению к Orobanchaceae) и Wightia. Палиноморфологические данные подтверждают филогенетические закономерности, выявленные в настоящее время у базальных Orobanchaceae и их ближайших родственников. Сделан вывод о том, что бороздно-оровый (возможно, 3-бороздно-оровый) тип пыльцевых зерен может быть предковым в семействе Orobanchaceae. Разнообразие пыльцы Orobanchaceae развилось на основе нескольких типов и подтипов, которые были свойственны гипотетическим предкам Orobanchaceae и, вероятно, сохранились у современных представителей Paulowniaceae и Lindenbergieae. The authors express their gratitude to James C. Solomon, Head Curator of the Missouri Botanical Garden Herbarium (MO; St. Louis, Missouri, USA), Tatyana V. Shulkina, and other staff members of MO, and to Nataliya M. Shyian, Head Curator of the National Herbarium of Ukraine (KW; herbarium of the M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine), for their cooperation and assistance in extracting pollen samples from herbarium specimens. Kind help and cooperation of Dmytro O. Klymchuk, Head of the Center of Electron Microscopy, and Vitaliy I. Sapsay, SEM operator (M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine), is greatly appreciated. The authors are grateful to anonymous reviewers for their detailed review of the manuscript, valuable comments and suggestions. en Інститут ботаніки ім. М.Г. Холодного НАН України Український ботанічний журнал Систематика, флористика, географія рослин Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae Паліноморфологічні особливості представників триб Lindenbergieae і Cymbarieae та еволюція пилку в базальних кладах Orobanchaceae Палиноморфологические особенности представителей триб Lindenbergieae и Cymbarieae и эволюция пыльцы в базальных кладах Orobanchaceae Article published earlier |
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Digital Library of Periodicals of National Academy of Sciences of Ukraine |
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DSpace DC |
| title |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae |
| spellingShingle |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae Tsymbalyuk, Z.M. Mosyakin, S.L. Систематика, флористика, географія рослин |
| title_short |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae |
| title_full |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae |
| title_fullStr |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae |
| title_full_unstemmed |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae |
| title_sort |
palynomorphological peculiarities of representatives of tribes lindenbergieae and cymbarieae and pollen evolution in early-branching lineages of orobanchaceae |
| author |
Tsymbalyuk, Z.M. Mosyakin, S.L. |
| author_facet |
Tsymbalyuk, Z.M. Mosyakin, S.L. |
| topic |
Систематика, флористика, географія рослин |
| topic_facet |
Систематика, флористика, географія рослин |
| publishDate |
2018 |
| language |
English |
| container_title |
Український ботанічний журнал |
| publisher |
Інститут ботаніки ім. М.Г. Холодного НАН України |
| format |
Article |
| title_alt |
Паліноморфологічні особливості представників триб Lindenbergieae і Cymbarieae та еволюція пилку в базальних кладах Orobanchaceae Палиноморфологические особенности представителей триб Lindenbergieae и Cymbarieae и эволюция пыльцы в базальных кладах Orobanchaceae |
| description |
Pollen morphology of four species belonging to four genera of the tribe Cymbarieae and two species of Lindenbergia of the
tribe Lindenbergieae (Orobanchaceae) was studied using light and scanning electron microscopy. Pollen grains in Lindenbergieae
are 3-colporate (rarely 2-colporate), prolate, spheroidal and oblate-spheroidal, small-sized, with reticulate exine sculpture.
Pollen grains in Cymbarieae are 3-colpate, rarely 4-colpate, prolate, spheroidal and oblate-spheroidal, medium-sized. Exine
sculpture in Cymbarieae is retipilate and rugulate-retipilate. Pollen characters of Cymbarieae and Lindenbergieae are compared
with pollen patterns in Paulowniaceae and crown clades of Orobanchaceae. The earliest-branching clade of Orobanchaceae
(Lindenbergieae) is palynomorphologically similar to Paulowniaceae (the clade sister to all Orobanchaceae) and to Wightia.
These palynomorphological findings confirm the phylogenetic patterns recently revealed in basal Orobanchaceae and their
closest relatives. It is concluded that the colporate (most probably 3-colporate) type of pollen grains could be ancestral in
Orobanchaceae. Pollen diversity in crown clades of Orobanchaceae evolved on the base of a few pollen types and subtypes, which
were peculiar to hypothetical ancestors of Orobanchaceae and are probably preserved in the extant taxa of Paulowniaceae and
Lindenbergieae.
З використанням світлової та сканувальної електрон- ної мікроскопії досліджено морфологію пилкових зерен чотирьох видів з чотирьох родів триби Cymbarieae та двох видів роду Lindenbergia триби Lindenbergieae (Orobanchaceae). Встановлено, що пилкові зерна триби Lindenbergieae 3-борозно-орові (зрідка 2-борозно-орові), еліпсоїдальні, сфероїдальні або сплющено-сфероїдальні за формою, дрібних розмірів, з сітчастою скульптурою екзини. Пилкові зерна триби Cymbarieae 3-борозні, зрідка 4-борозні, еліпсоїдальні, сфероїдальні або сплющено-сфероїдальні за формою, середніх або великих розмірів, з сітчасто-паличковою або зморшкувато-сітчасто-паличковою скульптурою екзини. Особливості пилкових зерен представників триб Cymbarieae і Lindenbergieae порівнюються з такими в Paulowniaceae і верхівкових кладах Orobanchaceae. Базальна клада Orobanchaceae (Lindenbergieae) за паліноморфологічними особливостями подібна до Paulowniaceae (сестринська клада до всіх Orobanchaceae) і Wightia. Паліноморфологічні висновки підтверджують філогенетичні закономірності, які виявлені у базальних Orobanchaceae та їхніх найближчих родичів. Зроблено висновок, що борозно-оровий (ймовірно, 3-борозно-оровий) тип пилкових зерен може бути предковим у родині Orobanchaceae. Різноманітність пилкових зерен у верхівкових кладах Orobanchaceae еволюціонувала на основі декількох типів і підтипів пилку, властивих гіпотетичним предкам Orobanchaceae; такі типи, ймовірно, збереглися в сучасних представників Paulowniaceae та Lindenbergieae.
С помощью световой и сканирующей электронной микроскопии изучены пыльцевые зерна четырех видов из четырех родов трибы Cymbarieae и двух видов рода Lindenbergia трибы Lindenbergieae (Orobanchaceae). Установлено, что пыльцевые зерна трибы Lindenbergieae 3-бороздно-оровые (изредка 2-бороздно-оровые), эллипсоидальные, сфероидальные или сплющено-сфероидальные по форме, мелких размеров, с сетчатой скульптурой экзины. Пыльцевые зерна трибы Cymbarieae 3-бороздные, изредка 4-бороздные, эллипсоидальные, сфероидальные или сплющено-сфероидальные по форме, средних или больших размеров, с сетчато-палочковой или морщинисто-сетчасто-палочковой скульптурой экзины. Особенности пыльцевых зерен представителей триб Cymbarieae и Lindenbergieae сравниваются с таковыми у Paulowniaceae и терминальных клад Orobanchaceae. Базальная клада в семействе Orobanchaceae (Lindenbergieae) по палиноморфологическим особенностям сходна с Paulowniaceae (сестринская клада по отношению к Orobanchaceae) и Wightia. Палиноморфологические данные подтверждают филогенетические закономерности, выявленные в настоящее время у базальных Orobanchaceae и их ближайших родственников. Сделан вывод о том, что бороздно-оровый (возможно, 3-бороздно-оровый) тип пыльцевых зерен может быть предковым в семействе Orobanchaceae. Разнообразие пыльцы Orobanchaceae развилось на основе нескольких типов и подтипов, которые были свойственны гипотетическим предкам Orobanchaceae и, вероятно, сохранились у современных представителей Paulowniaceae и Lindenbergieae.
|
| issn |
0372-4123 |
| url |
https://nasplib.isofts.kiev.ua/handle/123456789/176539 |
| citation_txt |
Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae and pollen evolution in early-branching lineages of Orobanchaceae / Z.M. Tsymbalyuk, S.L. Mosyakin // Український ботанічний журнал. — 2018. — Т. 75, № 2. — С. 123-136. — Бібліогр.: 42 назв. — англ. |
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123Укр. бот. журн., 2018, 75(2)
Introduction
The tribe Cymbarieae D. Don (Orobanchaceae Vent.) in
its current circumscription includes six or seven genera
and ca. 14 species of root hemiparasites (Fischer, 2004;
Bennett, Mathews, 2006; Reveal, 2012; McNeal et al.,
2013; Olmstead, 2016). The genera currently included in
the tribe are Bungea C.A. Mey. (2 species, southwestern
and Central Asia and China), Cymbaria L. sensu lato
(4 species, southeastern Europe, Central and eastern
Asia; many authors also include here Cymbochasma
(Endl.) Klokov & Zoz), Lesquereuxia Boiss. (1 species,
L. syriaca Boiss. & Reut. = Siphonostegia syriaca (Boiss.
& Reut.) Boiss., Eastern Mediterranean; most probably
nested in Siphonostegia: see McNeal et al., 2013),
Monochasma Maxim. ex Franch. & Sav. (4 species, East
Asia), Schwalbea L. (1 species, S. americana L., eastern
North America), and Siphonostegia Benth. (2 species:
S. chinensis Benth. and S. laeta S. Moore, East Asia;
or 3 species, if S. syriaca is included) (Fischer, 2004;
Bennett, Mathews, 2006; Takhtajan, 2009; McNeal
et al., 2013; Olmstead, 2016).
The genus Lindenbergia Lehm. is represented by
non-parasitic taxa and includes 12–15 species occurring
mostly in tropical regions, from northeastern Africa
through southern and southeastern Asia (including the
Himalayas) to Philippines (Mabberley, 1997; Stevens,
2001–onwards; Fischer, 2004; Olmstead, 2016).
In earlier variants of the system of A.L. Takhtajan
(1987, 1997) the mentioned genera Schwalbea,
Bungea, Siphonostegia, Cymbaria, and Monochasma
were included (with many other genera) in the tribe
Rhinantheae Lam. & DC. of Scrophulariaceae subfam.
Rhinanthoideae. In the latest version of his system,
Takhtajan (2009) placed the genera Schwalbea,
Cymbaria (including Cymbochasma), Siphonostegia,
Lesquereuxia, Bungea, Monochasma in the tribe
Cymbarieae (also with some other genera), and their
familial and subfamilial placement remained the same.
Fischer (2004) included in Cymbarieae six genera:
Schwalbea, Cymbaria (including Cymbochasma),
Siphonostegia, Lesquereuxia, Bungea, and Monochasma.
Takhtajan (1987, 1997) initially placed Lindenbergia
in Scrophulariaceae subfam. Scrophularioideae trib.
Gratioleae Benth. In 2009 he moved that genus to the
https://doi.org/10.15407/ukrbotj75.02.123
Palynomorphological peculiarities of representatives of tribes
Lindenbergieae and Cymbarieae and pollen evolution in early-branching
lineages of Orobanchaceae
Zoya M. TSYMBALYUK, Sergei L. MOSYAKIN
M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine
2 Tereshchenkivska Str., Kyiv 01004, Ukraine
palynology@ukr.net
Tsymbalyuk Z.M., Mosyakin S.L. Palynomorphological peculiarities of representatives of tribes Lindenbergieae and Cymbarieae
and pollen evolution in early-branching lineages of Orobanchaceae. Ukr. Bot. J., 2018, 75(2): 123–136.
Abstract. Pollen morphology of four species belonging to four genera of the tribe Cymbarieae and two species of Lindenbergia of the
tribe Lindenbergieae (Orobanchaceae) was studied using light and scanning electron microscopy. Pollen grains in Lindenbergieae
are 3-colporate (rarely 2-colporate), prolate, spheroidal and oblate-spheroidal, small-sized, with reticulate exine sculpture.
Pollen grains in Cymbarieae are 3-colpate, rarely 4-colpate, prolate, spheroidal and oblate-spheroidal, medium-sized. Exine
sculpture in Cymbarieae is retipilate and rugulate-retipilate. Pollen characters of Cymbarieae and Lindenbergieae are compared
with pollen patterns in Paulowniaceae and crown clades of Orobanchaceae. The earliest-branching clade of Orobanchaceae
(Lindenbergieae) is palynomorphologically similar to Paulowniaceae (the clade sister to all Orobanchaceae) and to Wightia.
These palynomorphological findings confirm the phylogenetic patterns recently revealed in basal Orobanchaceae and their
closest relatives. It is concluded that the colporate (most probably 3-colporate) type of pollen grains could be ancestral in
Orobanchaceae. Pollen diversity in crown clades of Orobanchaceae evolved on the base of a few pollen types and subtypes, which
were peculiar to hypothetical ancestors of Orobanchaceae and are probably preserved in the extant taxa of Paulowniaceae and
Lindenbergieae.
Keywords: Cymbarieae, Lindenbergieae, Orobanchaceae, pollen evolution, pollen morphology, phylogeny, taxonomy
© Z.M. TSYMBALYUK, S.L. MOSYAKIN, 2018
mailto:palynology@ukr.net
124 Ukr. Bot. J., 2018, 75(2)
studies (Bennett, Mathews, 2006; McNeal et al.,
2013), the clade of Cymbarieae is subdivided into
two subclades: one of these clades includes Bungea,
Cymbaria (including Cymbochasma), and Monochasma;
the other houses Siphonostegia (including Lesquereuxia)
and Schwalbea.
Our earlier studies and analysis of pollen morphology
in basal clades of Scrophulariaceae sensu stricto allowed
us to outline the main trends of morphological pollen
evolution in the family in its new circumscription and
to hypothesize on possible ancestral pollen types in the
group (Mosyakin, Tsymbalyuk, 2015, 2017). Because
of that, we may expect that a comprehensive analysis
of pollen morphology in early-branching clades of
Orobanchaceae could bring comparable results and shed
light on main trends of pollen evolution in that group
as well.
The purpose of the present research was to study and
analyze the morphological features of pollen grains of
representatives of Cymbarieae and Lindenbergieae in
the updated taxonomic circumscriptions of these tribes,
and to compare the pollen patterns with existing systems
and molecular phylogenetic data.
Materials and methods
Pollen of four species belonging to four genera of
Cymbarieae (Bungea, Cymbaria, Cymbochasma, and
Siphonostegia) was sampled in the National Herbarium
of Ukraine (KW – herbarium of the M.G. Kholodny
Institute of Botany, National Academy of Sciences of
Ukraine, Kyiv, Ukraine). Pollen grains of two species
of Lindenbergia were sampled in the herbarium of the
Missouri Botanical Garden (MO; St. Louis, Missouri,
USA). Data of the studied specimens are cited
exactly according to the label information, in English
translation and in original languages.
In general, the methods used in the present study
are essentially the same as those we used earlier (see
Mosyakin, Tsymbalyuk, 2015a, b, 2017). Pollen
morphology was studied using light microscopy and
scanning electron microscopy. For light microscopy
studies (LM, Biolar, × 700), the pollen was acetolyzed
following Erdtman (1952). For size determinations,
20 measurements were taken along the polar (P) and
equatorial (E) axes for each species. For scanning
electron microscopy (SEM, JSM-6060LA), pollen
grains were treated with 96%-ethanol, then these
samples were sputter-coated with gold and investigated
at the Center of Electron Microscopy of the
tribe Stemodieae Reveal, which was positioned in his
system close to Gratioleae, in the same subfamily. Fischer
(2004) placed Lindenbergia in Scrophulariaceae trib.
Stemodieae. Now the genus is placed in Orobanchaceae
trib. Lindenbergieae T. Yamaz. (= Lindenbergiaceae
Doweld, 2001).
Many authors studied and discussed pollen
morphology of representatives of Scrophulariaceae and
Orobanchaceae in general (Minkin, Eshbaugh, 1989),
or specifically Rhinantheae (Inceoğlu, 1982; Lu et al.,
2007; Tsymbalyuk, Mosyakin, 2017), and its taxonomic
and evolutionary significance (see also Tsymbalyuk,
Mosyakin, 2013a, b; Mosyakin, Tsymbalyuk, 2015a, b,
2017 and references therein). However, there are only
a few publications reporting data on pollen of taxa now
placed in Cymbarieae; these publications provide some
data based on light and scanning electron microscopy
(Inceoğlu, 1982; Minkin, Eshbaugh, 1989; Lu et al.,
2007). Pollen grains of two species (Bungea trifida and
Lesquereuxia syriaca) currently placed in Cymbarieae
were also studied using transmission electron microscopy
(Inceoğlu, 1982). However, no comprehensive analysis
of palynomorphological peculiarities of Cymbarieae in
its updated phylogeny-based circumscription has been
done until now.
Prijanto (1969) provided the following information
about pollen grains of Lindenbergia: "Pollen grains
small, 3-colporate, rarely 2-colporate, oblate spheroidal
to prolate spheroidal (polar axis 12–19 μm long,
equatorial diameter 13–18 μm; apocolpium diameter
3–5 μm; exine about 0.8–1.5 μm thick, sexine as thick
as nexine, reticulate". However, no images of pollen
grains were published by Prijanto (1969). Hjertson
(1995) updated the information of Prijanto (1969) and
provided SEM images of pollen grains of L. muraria
(Roxb. ex D. Don) Brühl and L. grandiflora (Buch.-
Ham. ex D. Don) Benth. He concluded that "pollen
grains in Lindenbergia are tricolporate, oblate to prolate
in shape, with a 12–19 μm long polar axis and an
equatorial diameter of 13–18 μm. The exine as well
as the sexine is about 1 μm thick, and the surface is
reticulate".
Molecular phylogenetic evidence indicate that
Cymbarieae is one of the early-branching (basal)
lineages of Orobanchaceae, most probably its second-
branching clade, following the basalmost clade of
Lindenbergia (Orobanchaceae trib. Lindenbergieae =
Lindenbergiaceae) (McNeal et al., 2013; Cusimano,
Wicke, 2016; Schneider et al., 2016; Schneider, Moore,
2017, etc.). According to molecular phylogenetic
125Укр. бот. журн., 2018, 75(2)
Type I — 3-colporate
Sculpture reticulate.
P = 13.3–18.6 µm, E = 13.3–18.6 µm.
Colpi long, narrow, 1.3–2.7 μm wide, with acute
ends.
Endoapertures mainly indistinct, circular, 2.4–2.7
µm long and wide.
Exine 0.7–1.6 µm. Lindenbergia philippensis,
L. sinaica.
Type II — 3-colpate
Subtype 1. Sculpture retipilate. Caput of pila 0.17–
0.33 µm.
P = 38.6–47.9 µm, E = 34.6–43.9 µm.
Colpi long, medium-width, 2.4–3.3 µm wide, ends
acute.
Exine 1.3–3.3 µm. Bungea trifida.
Subtype 2. Sculpture retipilate and rugulate-
retipilate. Caput of pila 0.41–0.67 µm.
P = 37.2–47.9 µm, E = 33.2–42.6 µm.
Colpi medium-length, wide, 4.0–6.6 µm wide, ends
blunt, sometimes acute.
Exine 1.6–2.7 µm. Cymbaria dahurica.
Subtype 3. Sculpture retipilate. Caput of pila 0.17–
0.25 µm.
P = 29.3–33.2 µm, E = 30.6–35.9 µm.
Colpi medium-length, medium-width, 2.7–5.3 µm
wide, ends blunt, indistinct.
Exine 0.7–1.3 µm. Cymbochasma borysthenica.
Subtype 4. Sculpture retipilate. Caput of pila 0.16–
0.25 µm.
P = 22.6–29.3 µm, E = 25.3–29.3 µm.
Colpi long, narrow, 1.3–2.4 µm wide, ends blunt.
Exine 1.3–2.4 µm. Siphonostegia chinensis.
Descriptions of pollen grains
Genus Lindenbergia Lehm.
Lindenbergia philippensis (Cham.) Benth. (Fig. 1,
a–c; Fig. 4, a–d)
LM. Pollen grains 3-colporate, oblate-spheroidal
and spheroidal, occasionally prolate, in polar view
3-lobate, in equatorial view elliptical and circular. P =
13.3–17.3 µm, E = 14.6–18.6 µm. Colpi long, narrow,
1.3–2.7 µm wide, with indistinct (some distinct) more
or less strict margins, tapering to acute ends; colpus
membrane smooth. Endoapertures indistinct, circular,
2.4–2.7 µm wide, 2.4–2.7 µm long. Mesocolpium =
9.3–10.6 µm, apocolpium = 2.7–4.0 (5.3) µm. Exine
1.1–1.6 µm thick. Tectum nearly equal to infratectum.
Columellae indistinct or distinct, thin. Exine sculpture
indistinct or distinct, microreticulate.
M.G. Kholodny Institute of Botany. The micrographs
were minimally edited with Adobe Photoshop 6.0 to
enhance the images.
Terminology used in descriptions of pollen grains
mainly follows the glossaries by Tokarev (2002) and Punt
et al. (2007) with some necessary minor adjustments.
General description of pollen grains
Lindenbergieae
Pollen grains in monads, radially symmetrical,
isopolar, 3-colporate (rarely 2-colporate, according
to Prijanto, 1969), prolate, spheroidal or oblate-
spheroidal; mainly small-sized: P = 13.3–18.6 µm
(12–19 μm, according to Prijanto, 1969), E = 13.3–
18.6 µm. Outline in polar view 3-lobate, in equatorial
view elliptical or circular. Colpi long, narrow, 1.3–
2.7 μm wide, with mainly indistinct (sometimes
distinct) more or less strict margins, with acute ends.
Endoapertures mainly indistinct, circular, 2.4–
2.7 µm long and wide. Exine 0.7–1.6 µm. Tectum
nearly equal to infratectum. Columellae indistinct or
distinct, thin, or exine layers invisible. Exine sculpture
reticulate. Colpus membrane smooth.
Cymbarieae
Pollen grains in monads, radially symmetrical,
isopolar, mainly 3-colpate, rarely 4-colpate, prolate,
spheroidal, or oblate-spheroidal. The outlines in
equatorial view elliptical or circular, in polar view
sub-circular, circular, and sub-triangular; medium- or
large-sized: P = 22.6–47.9 μm (up to 50 μm, according
to Lu et al., 2007), E = 25.3–43.9 μm. Colpi long or
medium-length, narrow, medium-width to wide, 1.3–
6.6 μm wide, with indistinct, uneven margins, and
blunt, acute, or indistinct ends. Exine 0.7–3.3 μm.
Tectum nearly equal to infratectum, columellae mainly
indistinct or thin and arranged more or less regularly.
Exine sculpture retipilate, rarely rugulate-retipilate.
Capita (pila heads) arranged in circle in most or all
regions of pollen surface. Caput of pila 0.16–0.67 μm
(up to 0.90 μm, according to Lu et al., 2007). Colpus
membrane granulate.
Pollen types and subtypes
Based on their aperture types, pollen grains of the
studied species belong to the same basic pollen types.
The second type (3-colpate) contains four subtypes
segregated according to their exine sculpture, pollen
size, details of colpi, and thickness of the exine.
126 Ukr. Bot. J., 2018, 75(2)
Doğubayazit. 1600 m. Pastures. Perennial. Flower flava
[sic!]. 30 May 1966. Davis, No 43867 (KW).
Genus Cymbaria L.
Cymbaria dahurica L. (Fig. 2, d–f; Fig. 5, e–h)
LM. Pollen grains 3-colpate, prolate and occasionally
oblate-spheroidal, in polar view sub-triangular, in
equatorial view elliptical. P = 37.2–47.9 µm, E = 33.2–
42.6 µm. Colpi medium-length, 4.0–6.6 µm wide, with
indistinct, uneven margins, tapering to blunt, sometimes
acute ends, colpus membrane smooth and granulate.
Mesocolpium = 26.6–33.2 µm, apocolpium = 10.6–
19.9 µm. Exine 1.6–2.7 µm thick. Tectum nearly equal
to infratectum. Columellae indistinct. Exine sculpture
indistinct, sometimes distinct, microreticulate.
SEM. Sculpture retipilate and rugulate-retipilate.
Caput of pila 0.41–0.67 µm. Colpus membrane
granulate.
Specimens investigated: 1. Khakassian Autonomous
Region [now Republic of Khakassia, Russian
Federation], Altai District, near Ochury village.
Southern rocky slope, fine-turfgrass steppe. 30 June
1969. A. Koroleva (KW) [Label in Russian: Хакасская
авт. обл., Алтайский р-н, окр. с. Очуры. Южный
каменистый склон, мелко-дерновинная степь.
30.VI 1969. А. Королева]. 2. Transbaikalia [now
Zabaykalsky Krai, Russian Federation]. On dry
mountain slopes and in steppes near Nerchinsk,
abundant. June 1898. Coll. Gubelman and Migunov
(KW) [Label in Russian: Забайкалье. На сухих
склонах гор и в степях около Нерчинска в изобилии.
Июнь 1898; Собр. Губельман и Мигунов].
Genus Cymbochasma (Endl.) Klokov & Zoz
Cymbochasma borysthenica (Pall. ex Schlecht.)
Klokov & Zoz (Cymbaria borysthenica Pall. ex Schlecht.)
(Fig. 3, a–c; Fig. 5, i–l)
LM. Pollen grains 3-colpate, occasionally 4-colpate,
oblate-spheroidal, in polar view sub-circular, in
equatorial view elliptical. P = 29.3–33.2 µm, E = 30.6–
35.9 µm. Colpi medium-length, medium-width, 2.7–
5.3 µm wide, with indistinct, uneven margins, tapering
to blunt, indistinct ends, colpus membrane smooth
and granulate. Mesocolpium = 22.6–26.6 µm,
apocolpium = 6.6–9.3 µm. Exine 0.7–1.3 µm thick.
Tectum nearly equal to infratectum. Columellae
indistinct. Exine sculpture indistinct, sometimes
distinct, microreticulate.
SEM. Sculpture retipilate. Caput of pila 0.17–
0.25 µm. Colpus membrane granulate.
SEM. Sculpture reticulate. Colpus membrane
smooth.
Specimen investigated: Philippines; Mountain
Province; Bontoc Municipality; Bontoc territory;
Caluttit; 17°05′ N, 120°58′ E; 1000 m elev. 17 November
1982. C.C. Bodner. No 131 (MO).
Lindenbergia sinaica Benth. (Fig. 1, d–f; Fig. 4, e–h)
LM. Pollen grains 3-colporate, prolate and
spheroidal, occasionally oblate-spheroidal, in polar
view 3-lobate, in equatorial view elliptical and circular.
P = 14.6–18.6 µm, E = 13.3–17.3 µm. Colpi long,
narrow, 2.0–2.4 µm wide, with indistinct (occasionally
some distinct) more or less strict margins, tapering to
acute ends; colpus membrane smooth. Endoapertures
indistinct, more or less circular, 2.7 µm wide, 2.4–
2.7 µm long. Mesocolpium = 7.9–10.6 µm, apocol-
pium = 4.0 µm. Exine 0.7–1.1 µm thick, exine layers
invisible. Exine sculpture indistinct, foveolate.
SEM. Sculpture reticulate. Colpus membrane
smooth.
Specimen investigated: [Ethiopia]. About 150 km.
SW of Assab [Eritrea], along road to Kombolcha
[Ethiopia]. Alt.: 400 m. Dry, rocky slope. 18.I 1966.
W. de Wilde. No 9771 (MO).
Genus Bungea C.A. Mey.
Bungea trifida (Vahl) C.A. Mey. (Fig. 2, a–c; Fig. 5,
a–d)
LM. Pollen grains 3-colpate, prolate and occasionally
spheroidal, in polar view sub-triangular and/or circular,
in equatorial view elliptical and circular. P = 38.6–
47.9 µm, E = 34.6–43.9 µm. Colpi long, medium-width,
2.4–3.3 µm wide, with indistinct, uneven margins,
tapering to more or less acute or indistinct ends; colpus
membrane granulate. Mesocolpium = 26.6–34.6 µm,
apocolpium = 6.6–13.3 µm. Exine 1.3–3.3 µm thick.
Tectum nearly equal to infratectum. Columellae
invisible. Exine sculpture indistinct, microreticulate.
SEM. Sculpture retipilate. Caput of pila 0.17–
0.33 µm. Colpus membrane granulate.
Specimens investigated: 1. Armenian SSR [now
Armenia], Vedi District [now in Ararat Province],
right slope of the Vedi River, between Azizkend and
Daynaz villages, phrygana. 27.V 1960. A. Takhtajan, E.
Gabrielian, L.I. Mulkijanian (KW) [Label in Russian:
Арм. ССР, Вединский р-н, правый борт р. Веди,
с.с. Азизкенд × Дайназ, фригана. 27.V 1960.
А. Тахтаджян, Э. Габриэлян, Л.И. Мулкиджанян].
2. Turkey. B 10 Kars: Pamuk Dağ, 20 km from Iğdir to
127Укр. бот. журн., 2018, 75(2)
a b
c d
e f
Fig. 1. Pollen grains of Lindenbergia (scanning electron microscopy): a–c – L. philippensis; d–f – L. sinaica; a – polar and
equatorial view; e – equatorial view; b–d, f – reticulate exine sculpture
128 Ukr. Bot. J., 2018, 75(2)
a b
c d
e f
Fig. 2. Pollen grains of Bungea and Cymbaria (scanning electron microscopy): a–c – B. trifida; d–f – C. dahurica; a, e –
equatorial view; b, c – retipilate exine sculpture; d, f – rugulate-retipilate exine sculpture
129Укр. бот. журн., 2018, 75(2)
a b
c d
e f
Fig. 3. Pollen grains of Cymbochasma and Siphonostegia (scanning electron microscopy): a–c – C. borysthenica; d–f –
S. chinensis; a, e – equatorial view; b–d, f – retipilate exine sculpture
130 Ukr. Bot. J., 2018, 75(2)
Specimens investigated: 1. Ukrainian SSR [now
Ukraine], Kherson Region, Kakhovka District,
between Lvovo [L'vove] and Kozatskoye [Kozats'ke]
villages, slopes of a large ravine of western exposition,
petrophilic steppe area, on limestone. 24 April 1972.
B.V. Zaverukha, No. 058169 (KW) [Label in Russian:
УССР, Херсонская обл., Каховский р-н, между
селами Львово – Козацкое, склоны большой
балки западной экспозиции, степной участок
петрофильного х-ра, на известняках. 24.IV 1972.
Б.В. Заверуха. № 058169]. 2. [Ukraine] Mykolayiv
Region, Snigurivka town, limestone slopes at the
Ingulets River. 20 April 1972. L. Krytzka, No. 040211
(KW) [Label in Ukrainian: Миколаївська обл.,
м. Снігурівка, вапнякові схили на р. Інгулець.
20.IV 1972. Л. Крицька. № 040211].
Genus Siphonostegia Benth.
Siphonostegia chinensis Benth. (Fig. 3, d–f; Fig. 5,
m–p)
LM. Pollen grains 3-colpate, oblate-spheroidal,
spheroidal, occasionally prolate, in polar view circular,
in equatorial view circular. P = 22.6–29.3 µm, E =
25.3–29.3 µm. Colpi long, narrow, 1.3–2.4 µm wide,
with indistinct, uneven margins, tapering to blunt ends,
colpus membrane granulate. Mesocolpium = 18.6–
22.6 µm, apocolpium = 5.3–9.3 µm. Exine 1.3–2.4 µm
thick. Tectum nearly equal to infratectum. Columellae
distinct, thin, arranged more or less regularly. Exine
sculpture distinct, microreticulate.
SEM. Sculpture retipilate. Caput of pila 0.16–
0.25 µm. Colpus membrane granulate.
Specimen investigated: [Russia, Russian Far
East] Primorye Province, near Khabarovsk city, in
sands. 11 July 1910. N. Desoulavi (KW) [Label in
Latin and Russian: Herbarium Florae Rossicae.
Prov. Primorskaja, pr. urb. Chabarowsk, in arenosis.
11.VII 1910. Н. Десулави].
Original and published data on quantitative and
qualitative pollen characters of representative of
Cymbarieae and Lindenbergieae are summarized in
Tables 1 and 2.
Comparative pollen morphology of genera of
Cymbarieae and Lindenbergieae
In general, our data are in good agreement with the
results of previous studies (Inceoğlu, 1982; Minkin,
Eshbaugh, 1989; Lu et al., 2007). Analysis of our original
palynomorphological data and literature records
demonstrated that pollen grains of representatives of all
genera of Cymbarieae are characterized by the 3-colpate
type of apertures, mainly with retipilate sculpture
(Table 2).
a b c d
e f g h
Fig. 4. Pollen grains of Lindenbergia (light microscopy): a–d – L. philippensis; e–h – L. sinaica; a, b, e, f – equatorial view;
c, d, g, h – polar view. Scale bars: 10 µm
131Укр. бот. журн., 2018, 75(2)
a b c d
e f g h
i j k l
m n o p
Fig. 5. Pollen grains of Bungea, Cymbaria, Cymbochasma, and Siphonostegia (light microscopy): a–d – B. trifida; e–h –
C. dahurica; i–l – C. borysthenica; m–p – S. chinensis. a, b, e, f, i, j, m, n – equatorial view; c, d, g, h, k, l, o, p – polar view.
Scale bars: 10 µm.
132 Ukr. Bot. J., 2018, 75(2)
Table 1. Summary of pollen morphometric features
Taxon
Polar axis
(µm)
Equatorial axis
(µm)
Colpi width
(µm)
Mesocolpium
(µm)
Apocolpium
(µm)
Exine (µm) Reference
Lindenbergia philippensis 13.3–17.3 14.6–18.6 1.3–2.7 9.3–10.6 2.7–4.0 (5.3) 1.1–1.6 original data
Lindenbergia sinaica 14.6–18.6 13.3–17.3 2.0–2.4 7.9–10.6 3.3–4.0 0.7–1.1 original data
Bungea trifida 38.6–47.9 34.6–43.9 2.4–3.3 26.6–34.6 6.6–13.3 1.3–3.3 original data
Bungea trifida 35 39 – – 7 1.1 Inceoğlu, 1982
Cymbaria dahurica 37.2–47.9 33.2–42.6 4.0–6.6 26.6–33.2 10.6–19.9 1.6–2.7 original data
Cymbaria dahurica 32.5–42.5 27.5–35.0 – – – – Lu et al., 2007
Cymbaria mongolica 37.5–50.0 30.0–40.0 – – – – Lu et al., 2007
Cymbochasma borysthenica 29.3–33.2 30.6–35.9 2.7–5.3 22.6–26.6 6.6–9.3 0.7–1.3 original data
Monochasma savatieri 32.5–43.8 27.5–41.3 – – – – Lu et al., 2007
Siphonostegia chinensis 22.6–29.3 25.3–29.3 1.3–2.4 18.6–22.6 5.3–9.3 1.3–2.4 original data
Siphonostegia chinensis 22.1 22.4 – – – – Minkin, Eshbaugh, 1989
Siphonostegia chinensis 22.5–30.0 23.8–32.5 – – – – Lu et al., 2007
Siphonostegia syriaca
(Lesquereuxia syriaca)
24 24 – – 11 0.8 Inceoğlu, 1982
Schwalbea americana 27.2 27.2 – – – – Minkin, Eshbaugh, 1989
Original data are those reported here and in Table 2; "–" means no data reported.
Table 2. Summary of pollen morphological characteristics
Taxon Apertures Shape Polar view Colpi
Colpus
membrane
Exine sculpture/
caput of pila
Reference
Lindenbergia
philippensis
3-colporate
oblate-spheroidal,
spheroidal (some prolate)
trilobate
long, narrow,
acute ends
smooth reticulate
original
data
Lindenbergia
sinaica
3-colporate
prolate, spheroidal (some
oblate-spheroidal)
trilobate
long, narrow,
acute ends
smooth reticulate
original
data
Bungea trifida 3-colpate prolate (some spheroidal)
sub-triangular,
circular
long, medium-width,
acute ends
granulate
retipilate,
0.17–0.33
original
data
Bungea trifida 3-colpate oblate-spheroidal semi-angular long, acute ends
coarsely
granulate
retipilate
Inceoğlu,
1982
Cymbaria dahurica 3-colpate
prolate (some oblate-
spheroidal)
sub-triangular
medium-length,
wide, blunt or acute
ends
granulate
retipilate,
rugulate-retipilate,
0.41–0.67
original
data
Cymbaria dahurica 3-colpate subprolate sub-triangular
wide at equator and
narrow near poles
with
granules
retipilate,
0.45–0.90
Lu et al.,
2007
Cymbaria mongolica 3-colpate subprolate sub-triangular
narrow, long and
sunken
with
granules
retipilate,
0.16–0.40
Lu et al.,
2007
Cymbochasma
borysthenica
3-colpate
(some
4-colpate)
oblate-spheroidal sub-circular
medium-length,
medium-width,
blunt, indistinct ends
granulate
retipilate,
0.17–0.25
original
data
Monochasma
savatieri
3-colpate
prolate, spheroidal (some
oblate-spheroidal)
circular
wide at equator and
narrow near poles
with fine
granules
retipilate,
0.19–0.39
Lu et al.,
2007
Siphonostegia
chinensis
3-colpate
spheroidal, oblate-
spheroidal (some prolate)
circular
long, narrow, blunt
ends
granulate
retipilate,
0.16–0.25
original
data
Siphonostegia
chinensis
3-colpate spheroidal – – – retipilate
Minkin,
Eshbaugh,
1989
Siphonostegia
chinensis
3-colpate spheroidal circular
wide at equator, but
not narrow near poles
with coarse
granules
retipilate,
0.18–0.31
Lu et al.,
2007
Siphonostegia syriaca
(Lesquereuxia
syriaca)
3-colpate prolate, spheroidal circular long, acute ends
coarsely
granulate
retipilate
Inceoğlu,
1982
Schwalbea
americana
3-colpate spheroidal – – – retipilate
Minkin,
Eshbaugh,
1989
133Укр. бот. журн., 2018, 75(2)
the exine is thinner (0.7–1.1 µm thick), and exine layers
are invisible (indistinct).
Comparison of palynomorphological and molecular
phylogenetic evidence
According to molecular phylogenetic studies
(Bennett, Mathews, 2006; McNeal et al., 2013), the
clade of Cymbarieae is subdivided into two subclades.
The subclade that includes Bungea, Cymbaria,
Cymbochasma, and Monochasma is characterized by
larger pollen grains and wider colpi, as compared to the
subclade of Siphonostegia (including Lesquereuxia) and
Schwalbea.
The earliest-branching clade of Lindenbergia is
sister to the clade containing all other members of
Orobanchaceae. Small-sized 3-colporate pollen grains
with reticulate exine revealed in all studied taxa of
Lindenbergia are similar to pollen of some representatives
of Plantaginaceae, in particular, those of Gratioleae
(Tsymbalyuk, Mosyakin, 2013a, 2014; Tsymbalyuk,
2016). In our opinion, that superficial similarity does
not reflect direct phylogenetic relationships of these
taxa, but rather some recurrent patterns (plesiomorphic
characters) appearing is several clades of Lamiales.
The genus Paulownia Siebold & Zucc. is
currently placed phylogenetically as a group sister to
Orobanchaceae (Olmstead et al., 2001; Oxelman et al.,
2005; Bennet, Mathews, 2006; Schäferhoff et al., 2010;
McNeal et al., 2013). Pollen grains of Paulownia are
3-colporate, with reticulate exine (Erdtman, 1952;
Chen, 1983; Tsymbalyuk, 2014). In these characters,
Paulownia is rather similar to Lindenbergia. However,
Paulownia differ from Lindenbergia in having
small- and medium-sized pollen grains (small in
Lindenbergia), trilobate and sub-triangular in outline
(only trilobate in Lindenbergia), with distinct orae
(indistinct in Lindenbergia) and the colpus membrane
smooth and granulate (only smooth in Lindenbergia).
Some similarity with pollen of Paulownia and
Lindenbergia is also observed in pollen grains of the
phylogenetically still problematic genus Wightia Wall.
(Zhou et al. 2014), which also has 3-colporate pollen
with reticulate exine sculpture (Wei, 1989; Tsymbalyuk,
2014, 2016). However, in Paulownia and Lindenbergia
orae are circular and colpi are tapered to acute ends,
while Wightia has eliptical orae and colpi expanded to
rounded ends.
Thus, the earliest-branching clade of Orobanchaceae
(Lindenbergieae) is palynomorphologically similar to
the clade sister to all Orobanchaceae (Paulowniaceae)
Pollen grains in Cymbochasma borysthenica are
3-colpate and occasionally 4-colpate (Tsymbalyuk,
2011). They have the thinnest exine (0.7–1.3 μm)
among pollen grains of the studied species of the tribe.
Pollen grains of Cymbochasma borysthenica are smaller
as compared to pollen of Cymbaria dahurica and
C. mongolica, and also differ from species of Cymbaria
sensu stricto in the pollen shape and outline (see
Table 2). Thus, pollen characters may provide additional
evidence in favor of recognition of Cymbochasma as a
separate genus.
The two studied species of Cymbaria sensu stricto are
similar in their pollen size, shape, and outline; however,
they differ in their colpi structure and exine sculpture.
In pollen grains of Cymbaria dahurica, colpi are
medium-length, wider than in C. mongolica, and exine
sculpture is retipilate (caput of pila 0.41–0.90 μm) or
rugulate-retipilate, while C. mongolica has narrower and
longer colpi (as compared to those in C. dahurica) and
retipilate exine sculpture (caput of pila 0.16–0.40 μm)
(Lu et al., 2007, and original data).
In general, pollen grains of Bungea trifida and
Cymbaria mongolica (Lu et al., 2007) are similar in
their shape, outline, size, and exine sculpture; however,
Bungea trifida has colpi wider than those in C. mongolica,
and the thickest exine (1.3–3.3 μm) among all studied
species.
The smallest sizes are characteristic of pollen grains
of Siphonostegia chinensis (Table 1). This species also
has the narrowest colpi among all studied species.
Columellae in all species studied here are mainly
indistinct, while in Siphonostegia chinensis those are
distinct, thin, and arranged more or less regularly.
Pollen grains of Siphonostegia syriaca (Lesquereuxia
syriaca) (Inceoğlu, 1982) and S. chinensis are similar in
their shape, outline, size, exine sculpture, and length of
colpi; however, in S. syriaca the colpi ends are acute,
while in S. chinensis they are obtuse (with blunt ends).
Pollen grains of Schwalbea (Minkin, Eshbaugh,
1989) are similar to those of Siphonostegia in their
outline, size, and exine sculpture. Unfortunately, the
characters reported by Minkin and Eshbaugh (1989) are
insufficient for a more detailed comparative analysis.
The two studied species of Lindenbergia are similar
to each other in having the 3-colporate aperture
type, reticulate exine sculpture, and long and narrow
colpi. They, however, differ by the exine thickness:
in L. philippensis the exine is 1.1–1.6 µm thick,
the tectum is nearly equal to the infratectum, and
columellae are indistinct or distinct, while in L. sinaica
134 Ukr. Bot. J., 2018, 75(2)
Acknowledgements
The authors express their gratitude to James C. Solomon,
Head Curator of the Missouri Botanical Garden Herbarium
(MO; St. Louis, Missouri, USA), Tatyana V. Shulkina, and
other staff members of MO, and to Nataliya M. Shyian, Head
Curator of the National Herbarium of Ukraine (KW; herbarium
of the M.G. Kholodny Institute of Botany, National Academy
of Sciences of Ukraine), for their cooperation and assistance
in extracting pollen samples from herbarium specimens.
Kind help and cooperation of Dmytro O. Klymchuk, Head
of the Center of Electron Microscopy, and Vitaliy I. Sapsay,
SEM operator (M.G. Kholodny Institute of Botany, National
Academy of Sciences of Ukraine), is greatly appreciated. The
authors are grateful to anonymous reviewers for their detailed
review of the manuscript, valuable comments and suggestions.
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136 Ukr. Bot. J., 2018, 75(2)
вірно, 3-борозно-оровий) тип пилкових зерен може
бути предковим у родині Orobanchaceae. Різноманітність
пилкових зерен у верхівкових кладах Orobanchaceae ево-
люціонувала на основі декількох типів і підтипів пилку,
властивих гіпотетичним предкам Orobanchaceae; такі
типи, ймовірно, збереглися в сучасних представників
Paulowniaceae та Lindenbergieae.
Ключові слова: Cymbarieae, Lindenbergieae, Orobanchaceae,
еволюція пилку, морфологія пилку, систематика,
філогенія
Цымбалюк З.Н., Мосякин С.Л. Палиноморфологические
особенности представителей триб Lindenbergieae и
Cymbarieae и эволюция пыльцы в базальных кладах
Orobanchaceae. Укр. бот. журн., 2018, 75(2): 123–136.
Институт ботаники им. Н.Г. Холодного НАН Украины
ул. Терещенковская, 2, Киев 01004, Украина
С помощью световой и сканирующей электронной
микроскопии изучены пыльцевые зерна четырех ви-
дов из четырех родов трибы Cymbarieae и двух видов
рода Lindenbergia трибы Lindenbergieae (Orobanchaceae).
Установлено, что пыльцевые зерна трибы Lindenbergieae
3-бороздно-оровые (изредка 2-бороздно-оровые), эл-
липсоидальные, сфероидальные или сплющено-сфе-
роидальные по форме, мелких размеров, с сетча-
той скульптурой экзины. Пыльцевые зерна трибы
Cymbarieae 3-бороздные, изредка 4-бороздные, эллип-
соидальные, сфероидальные или сплющено-сферои-
дальные по форме, средних или больших размеров, с
сетчато-палочковой или морщинисто-сетчасто-палоч-
ковой скульптурой экзины. Особенности пыльцевых
зерен представителей триб Cymbarieae и Lindenbergieae
сравниваются с таковыми у Paulowniaceae и терминаль-
ных клад Orobanchaceae. Базальная клада в семействе
Orobanchaceae (Lindenbergieae) по палиноморфологиче-
ским особенностям сходна с Paulowniaceae (сестринская
клада по отношению к Orobanchaceae) и Wightia. Пали-
номорфологические данные подтверждают филогенети-
ческие закономерности, выявленные в настоящее время
у базальных Orobanchaceae и их ближайших родственни-
ков. Сделан вывод о том, что бороздно-оровый (возмож-
но, 3-бороздно-оровый) тип пыльцевых зерен может
быть предковым в семействе Orobanchaceae. Разно-
образие пыльцы Orobanchaceae развилось на основе не-
скольких типов и подтипов, которые были свойственны
гипотетическим предкам Orobanchaceae и, вероятно, со-
хранились у современных представителей Paulowniaceae
и Lindenbergieae.
Ключевые слова: Cymbarieae, Lindenbergieae,
Orobanchaceae, эволюция пыльцы, морфология пыльцы,
систематика, филогения
Tsymbalyuk Z.M., Mosyakin S.L. Ukr. Bot. J., 2017, 74(4):
310–325. [Цимбалюк З.М., Мосякін С.Л. Паліно-
морфологічні особливості представників триби
Rhinantheae (Orobanchaceae) у світлі молекулярно-
філогенетичних даних. Укр. бот. журн., 2017, 74(4):
310–325]. https://doi.org/10.15407/ukrbotj74.04.310.
Wei Zh.X. Pollen morphology of Wightia and its taxonomic
significance. Acta Bot. Yunnan., 1989, 11(1): 65–70.
[In Chinese, with English abstract].
Zare G., Dönmez A.A., Dönmez E.O. Pollen morphology
and evolution in the genus Orobanche L. s. l. and its
allied genera (Orobancheae/Orobanchaceae) in Turkey.
Pl. Syst. Evol., 2014, 300(5): 783–802. https://doi.
org/10.1007/s00606-013-0919-2.
Zhou Q.-M., Jensen S.R., Liu G.-L., Wang Sh., Li H.-Q.
Familial placement of Wightia (Lamiales). Pl. Syst. Evol.,
2014, 300(9): 2009–2017. https://doi.org/10.1007/
s00606-014-1029-5.
Recommended for publication Submitted 10.02.2018
by D.V. Dubyna
Цимбалюк З.М., Мосякін С.Л. Паліноморфологічні
особливості представників триб Lindenbergieae і
Cymbarieae та еволюція пилку в базальних кладах
Orobanchaceae.
Укр. бот. журн., 2018, 75(2): 123–136.
Інститут ботаніки ім. М.Г. Холодного НАН України
вул. Терещенківська, 2, Київ 01004, Україна
З використанням світлової та сканувальної електрон-
ної мікроскопії досліджено морфологію пилкових
зерен чотирьох видів з чотирьох родів триби Cymba-
rieae та двох видів роду Lindenbergia триби Lindenbergieae
(Orobanchaceae). Встановлено, що пилкові зерна триби
Lindenbergieae 3-борозно-орові (зрідка 2-борозно-орові),
еліпсоїдальні, сфероїдальні або сплющено-сфероїдальні
за формою, дрібних розмірів, з сітчастою скульптурою
екзини. Пилкові зерна триби Cymbarieae 3-борозні, зрід-
ка 4-борозні, еліпсоїдальні, сфероїдальні або сплющено-
сфероїдальні за формою, середніх або великих розмірів,
з сітчасто-паличковою або зморшкувато-сітчасто-па-
личковою скульптурою екзини. Особливості пилкових
зерен представників триб Cymbarieae і Lindenbergieae
порівнюються з такими в Paulowniaceae і верхівкових
кладах Orobanchaceae. Базальна клада Orobanchaceae
(Lindenbergieae) за паліноморфологічними особливостя-
ми подібна до Paulowniaceae (сестринська клада до всіх
Orobanchaceae) і Wightia. Паліноморфологічні висновки
підтверджують філогенетичні закономірності, які ви-
явлені у базальних Orobanchaceae та їхніх найближчих
родичів. Зроблено висновок, що борозно-оровий (ймо-
https://doi.org/10.15407/ukrbotj74.04.310
https://doi.org/10.1007/s00606-013-0919-2
https://doi.org/10.1007/s00606-013-0919-2
https://doi.org/10.1007/s00606-014-1029-5
https://doi.org/10.1007/s00606-014-1029-5
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