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Morphological characters of the seed coat in selected species of the genus Hypericum L. and their taxonomic value

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Eight Hypericum species are native to Poland: H. elegans Stephan ex Willd., H. hirsutum L., H. humifusum L., H. maculatum Crantz, H. montanum L., H. perforatum L., H. pulchrum L., and H. tetrapterum Fr. Only seeds of H. elegans were investigated in detail in Poland before, so here we present results of qualitative and quantitative analyses of seed morphology of the other 7 species, based on characters like seed length, width, and shape, seed coat sculpture, shape of epidermal cells of the testa, and number of epidermal cells along the seed axis. The results show that seeds of the studied species are small, 0.56-1.15 mm long and 0.26-0.49 mm wide. In SEM images, seed coat sculpture is reticulate in 5 species, papillate in H. hirsutum, and cup-shaped in H. pulchrum. The differences are caused by the varied final development of the testa epidermis, which constitutes the outer layer of the seed coat. The mean number of epidermal cells along the seed axis ranges from 22 to 33. Results of cluster analysis, based on the agglomeration method and including also published data on seeds of H. elegans, show that the variation in the investigated characters of seeds is reflected in the taxonomic division of the genus into sections.
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©
BRC




Hypericum 




Abstract.Hypericum   H. elegans  H. hirsutum  H. humifusum 
H. maculatum  H. montanum  H. perforatum L. H. pulchrum H. tetrapterum H. elegans




H. hirsutumH. pulchrum

H. elegans
 
Key words:
 
1. Introduction
Hypericum
 
ü



  Hypericum 


 Hypericum



   
Hypericum






    
   
   





 

et al.


 Hypericum   
      


H. elegans

Fig. 1.Hypericum
H. hirsutumH. humifusumH. maculatumH. montanumH. perforatumH. pulchrumH. tetrapterum
 

Hypericum 
i
ii

iii

2. Material and methods
 
Hypericum
H. hirsutum  H. humifusum  H. maculatum 
H. montanum  H. perforatum L. H. pulchrum 
H. tetrapterum 



H
pulchrum 
et
al. 
 

    
    
   

  
  


    


Table 1.Hypericum
  
H. hirsutum  
H. humifusum 



H. maculatum  
H. montanum  
H. perforatum  
H. pulchrum  
H. tetrapterum 



Hypericum 
3
Fig. 2.Hypericum


 


    

 2013).    

   
   









  H. elegans

    


3. Results

Hypericum 
 Hyperi-
cum





  H. humifusum 
H. perforatum and H. pulchrum

H. perfora-
tum and H. pulchrum


 




Hypericum hirsutum
  





  


    




Fig. 3.Hypericum

 H. hirsutum  H. humifusum  H. macula-
tumH. montanumH. perforatum H. pulchrumH.
tetrapterum
A B
 
 

Hypericum 


Hypericum humifusum 
    






   
  



Hypericum maculatum 
   










Hypericum montanum 
    




   

   
    


Hypericum perforatum 
   
  
  












Hypericum pulchrum
    
   
   



   
   



 


Hypericum tetrapterum 
Hypericum acutum 
 




    






 


H. hirsutum and H. pulchrum
H. humifusum




     
Hypericum



H. hirsutum
H. pulchrum

Fig. 4.Hypericum

  H. hirsutum  H. humifusum H. macula-
tumH. montanum H. perforatumH. pulchrum H.
tetrapterum
A B
 
 

Hypericum 
Fig. 5.Hypericum
  H. hirsutum  H. humifusum H. macula-
tumH. montanum H. perforatumH. pulchrum H.
tetrapterum
A B
 


H. humifusum
3
   
H. perforatum


   
H. tetrapterum
    

H. montanum
H. maculatum

H. elegans
Table 2.Hypericum  
 
(

 
H. elegans   
H. hirsutum   
H. humifusum   
H. maculatum   
H. montanum   
H. perforatum   
H. pulchrum   
H. tetrapterum   

Fig. 6.Hypericum
H. elegansH. hirsutumH. humifusumH. maculatumH. montanumH. perforatumH. pul-
chrumH. tetrapterum
4. Discussion
    
Hypericum


on Hypericum 
  




H
maculatum and H. hirsutum  
     

Hypericum 





   


   


 

H. hirsutum and
H. pulchrum  Taeniocarpium
H. humifusum
Oligostema    
Hypericum H. mon-
tanum  Adenosepalum 





 
Hy-
pericum 
   

References
Alonso M. A., Agulló J. C., VillAr J. l., JuAn A. & Crespo
M. B.Hyperi-
cum ericoidesHCoridium

Bojňanský V. & FargašoVá a.
  

CroCkett s. & roBson n.  
  Hypericum 


HAgeMAnHypericum empetri-
folium     

kaźmierCzakowa r., BloCh-orłowska j., Celka z., Cwener
a., DajDok z., miChalska-hejeDuk D., Pawlikowski
P., szCzęśniak e. & ziarnek k. 2016. 


mártonFi P. 2008. Hypericum dubium   

meseguer a. s. & sanmartín i.
Hypericum   
   

nürk
Hypericum 


nürk n. m. & Blattner F. r.  
 Hypericum 
 
roBson n. k. B.Hypericum 
  


roBson n. k. B.Hypericum


roBson n. k. B.Hypericum
MyriandraElodes.

roBson n. k. B.Hypericum
 Hypericum 
HypericumHypericum

roBson n. k. B.Hypericum 
Olympia 
Crossophyllum.  
roBson n. k. B.    Hypericum
  Hirtella  
Coridium 
statsoFt, inC.
 

steVensk. kuBitzki


szkuDlarzHyperi-
cum elegans

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... A particularly important feature is the sculpture of the seed coat and cell arrangement of its outer layer. However, only a relatively small number of Hypericum species have been studied so far in terms of seed morphology (Meseguer & Sanmartín 2012;Alonso et al. 2013;Szkudlarz & Celka 2016) and information about the anatomical structure of seeds in this genus has been also very limited (Szabes & Moro- zowa 1991;Matzk et al. 2001;Szkudlarz 2014). ...
... In Poland, all native Hypericum species were investigated in detail in terms of their seed morphology (Szkudlarz 2014;Szkudlarz & Celka 2016) and in case of H. elegans also anatomically (Szkudlarz 2014). A new species -H. ...
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Hypericum majus (A. Gray) Britton is an alien species for Europe. It originates from North America and, in recent years, has been spreading in Europe. Presently, this species is found in Germany, France, Italy, Bosnia and Herzegovina, and Belarus. In Poland, it was noted for the first time in 2017 in western part of the country. Thus far, no detailed morphology and anatomy of H. majus seeds based on light and electron microscopy studies has been presented. Considering the fact that seeds provide important taxonomical information and the discussed species has not been investigated in this respect, in this research, an attempt was made to broaden the present knowledge. Investigations were conducted based on samples originating from three localities in Central Europe (Poland). The obtained results showed that H. majus seeds are very small – about 0.5 mm in length. In the SEM image, their surface is reticulate, typical of majority of species in this genus. Anatomical analysis showed that seed coat of matured seeds is very delicate, composed of two cell layers with strongly lignified walls.
... The subsect. Fruit and seed traits play a significant role in the taxonomy of many species (Stace 1989;Szkudlarz 2009;Davitashvili & Karrer 2010;Szkudlarz & Celka 2016). The morphology and micromorphology of seeds are often utilised for taxonomic purposes also in Plantaginaceae and related families, like Scrophulariaceae or Orobanchaceae (e.g.: Elisens & Tomb 1983;Dong et al. 2015;Richardson Ahedor & Elisens 2015). ...
... Many authors highlighted the systematic value of the structural form of the seed coat due to its low phenetic variation of the species (e.g.: Barthlott 1981;Elisens & Tomb 1983;Martinez-Ortega & Rico 2001;Muñoz-Centeno et al. 2006, 2007Szkudlarz 2009;Szkudlarz & Celka 2016). The use of SEM made it possible to determine general types of seed coat sculpturing. ...
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The study was conducted on five species of Veronica L. subsection Agrestes occurring in Central Europe: Veronica agrestis L., V. polita Fr., V. opaca Fr., V. persica Poir. and V. filiformis Sm. These species are very similar morphologically and are often misidentified. Last thorough studies of morphology and micromorphology of their seeds were conducted in 1960s. Based on 48 herbarium specimens, we examined SEM images of 422 seeds. We found that 22 of the 30 studied morphological traits differentiated five species at statistical level and V. agrestis and V. persica differed with the greatest number of features from other species. Our measurements of seed size were not fully congruent with previous studies, suggesting dependence of these features on external conditions. Seeds were usually cochlidiospermous and ovoid with a reticulate-verrucate seed coat, but these features were, at the same time, quite variable. The results of discriminant function confirmed that some characters of the seed size, shape and coat sculpture could be taxonomically useful in distinguishing species of Veronica subsect. Agrestes . In addition, we believe that similarity of the examined seeds may confirm unity of this group and the need of identifying a subsection.
... The seed coat was covered by abundant superficial sculptures. The anatomical and ontogenetic characteristics of seed microsculptures could be used for taxonomic identification of plant species (Schenk et al. 2013;Szkudlarz and Celka, 2016). According to previous morphological and ultrastructural studies of the seed coat (Fredes et al., 2016), the seed coat sculpture development in Z. fabago could be divided into the following stages: ...
Article
Abstract: The ontogeny of seed coat and endosperm tissue in Zygophyllum fabago L. was studied to determine their developmental importance using different histochemical and microscopic techniques. Our results revealed that the ovule of Z. fabago was of the anatropous and bitegmic type. The inner epidermis cells were retained up to the end of seed development, whereas the other layers were removed in the early stages. Moreover, the outer integument was changed into the seed coat sculptures during the seed development. Concurrently, multiple cytoplasmic strings were formed at the seed coat cells. Fluorescence microscopic analysis indicated that callose and polyphenols were laid down at these strings. In the late stages of the seed development, the nucleus and cytoplasm of the cells were degenerated and the sculptures became obvious on the seed coat. The seed coat sculptures may play a role in the seed dispersal by wind. During the early developmental stages, the endosperm was of the nuclear type and then changed into the cellular type. Cytochemical tests indicated that in the later stages of seed development, the formation of starch grains and the thickening of cell walls occurred, causing considerable reduction of cell cavities as well as hardening the tissue. The cell storage in the endosperm tissue was more lipidbased than protein-based. Generally, due to the degeneration of the outer integument and the existence of the thin inner integument, the endosperm cell wall seemed to be thickened to protect the embryo and to save carbohydrates. The obtained results shed more light on the development of seed tissues in the family Zygophillaceae.
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The seed morphology of 40 taxa within the genus Hypericum (Hypericaceae) from China, representing 9 sections of the genus, was examined using both Light and Scanning Electron Microscopy to evaluate the taxonomic relevance of macro‐ and micro‐morphological features. Details articulating variation in seed size, color, shape, appendages, and seed coat ornamentation are described, illustrated, and compared, and their taxonomic importance is discussed. Seeds were generally brown in color and cylindric‐ellipsoid to prolonged cylindric in shape. Seed size displayed wide variation, ranging from 0.37–1.91 mm in length and 0.12–0.75 mm in width. Seed appendages were observed as a characteristic morphological feature. Seed surface ornamentation has high phenotypic plasticity, and four types (reticulate, foveolate, papillose, and ribbed) can be recognized. In general, seed color and shape have limited taxonomic significance. However, some other features represent informative characters that can be used efficiently in distinguishing the studied taxa at the section and/or species levels. The findings illustrate that considerable taxonomic knowledge can be obtained by investigating the seed features of Hypericum, and the use of Scanning Electron Microscopy can reveal inconspicuous morphological affinities among species and play a role in taxonomic and systematic studies of the genus Hypericum. Research Highlights Macro‐ and micro‐morphological features of seeds of 40 Hypericum taxa from China were examined using Light and Scanning Electron Microscopy, providing the first broad study regarding seed morphology for Hypericum from China. Details and variations of seed size, shape, color, surface ornamentation, and appendages are fully presented. Seed features and their variation have important taxonomic significance at the section and/or species levels within Hypericum.
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Здійснено дослідження паліноморфологічних особливостей шести видів роду Hypericum флори України H. аlpigenum, H. elegans, H. hirsutum, H. maculatum, H. montanum, H. perforatum. Всі досліджені види є цінними лікарськими рослинами, однак офіційно допускається використання сировини лише двох видів: H. perforatum та H. maculatum. Сировина інших видів також може збиратися з природних місцезростань, оскільки вони мають значне поширення в деяких регіонах України та морфологічно подібні до фармакопейних, їх домішка до сировини фармакопейних видів знижує її якість. Метою досліджень було здійснити порівняльний морфологічний аналіз пилкових зерен шести видів роду Hypericum флори України для з’ясування спільних і відмінних ознак, які дозволять ідентифікувати сировину цих видів. В результаті проведених паліноморфологічних досліджень встановлено, що пилкові зерна всіх шести видів роду Hypericum флори України дрібні, три-борозно-порові, еліпсоїдальні або сфероїдальні, в обрисах з полюса – трилопатеві, округло-трикутні, з екватора – еліптичні. В усіх досліджених видів борозни довгі, переважно з чіткими краями, загостреними кінцями та зернистою мембраною. Пори нечіткі. Ультраструктура екзини в досліджених видів роду Hypericum флори України дрібносітчаста (H. perforatum, H. alpigenum) та сітчаста (всі інші досліджені види). Морфометричні ознаки пилкових зерен досліджених видів: довжина полярної вісі, екваторіальний діаметр, ширина борозни, ширина мезокольпіума, діаметр апокольпіума, співвідношення довжини полярної вісі та екваторіального діаметру, ширини мезокольпіума та ширини апертур можна використовувати як додаткові діагностичні ознаки при ідентифікації видів роду Hypericum флори України.
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‘Dust seeds’ with an undifferentiated (organless) embryo are known to be produced by mycoheterotrophic species (MH) in nine families of angiosperms. However, aside from the numerous studies on seed germination of orchids, relatively little is known about germination in MH families. In the Ericaceae, some degree of mycoheterotrophy (full, partial or initial) and dust seeds with an undifferentiated embryo occur in all species in the three tribes of Monotropoideae, the only subfamily of Ericaceae with this combination of characters. In most species, the seed is <0.90 mm in the greatest dimension, the endosperm is absent ( Pityopus ) or consists of few to many (30–40) cells, and the embryo is minute, consisting of as few as two cells in Monotropa . Germination in Monotropoideae is monopolar, with only the radicular pole of the embryo participating in germination. Thus, germination polarity differs from that of the dust seeds of orchids in which only the plumular pole of the embryo (protocorm) participates in germination. The dust seeds in Monotropoideae require the presence of fungi, either direct contact with a fungus or the presence of a diffusible substance therefrom, to germinate (symbiotic germination). Recently, representatives of the four genera of tribe Pyroleae have been successfully germinated asymbiotically in vitro . We present a broad overview of dust-size seeds in angiosperms and conclude that they should be subdivided into at least two major categories.
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Hypericum is a worldwide‐distributed genus with almost 500 species, including the medically used, facultative apomictic species H. perforatum. It is one of the few large plant genera for which alpha taxonomy has been completed and most species have been described. To conduct a formal cladistic analysis of the genus, we coded 89 morphological characters for all described taxa and analyzed the data for the species using parsimony and Bayesian methods. The obtained trees indicate that Hypericum is monophyletic if the monotypic genus Santomasia is included, and that Lianthus is its sister. The arrangement of the remaining genera of Hypericaceae included in the analysis is in congruence with molecular phylogenies. Within Hypericum the cladistic analysis revealed a basal grade containing Mediterranean species and three big clades containing most of the diversity of the genus. In contrast to earlier assumptions, we found no indication for an African origin of Hypericum, but assume that the genus evolved in what today is the Mediterranean area. Our phylogenies indicate a shrubby habit to be the ancestral state within Hypericum from which species with tree‐like and herbaceous habit evolved, and that apomixis originated at least three times independently within the genus.
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The Carpathian flora occurs not only in the Carpathian Mountains, but also in large lowlands extending towards the south, north and east and involves introduced and invading flora of more than 7,500 species. Since the morphological characteristics of the seeds are usually constant they are very important for determination of systematic units. The present atlas of seeds with nearly 4,800 seed illustrations is supplemented with detailed seed descriptions, brief plant descriptions, locality and the native source of plants. This publication is unique, both in its extent – with so many plant seeds from such a wide-ranging region - and in the form of its presentation – with such detailed descriptions.
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Part 5(1) of this monographic series of papers on the genus Hypericum contains treatments of Section 10. Olympia and its relatives (Sections 11. Campylopus-16. Crossophyllum), which form a Euro-Mediterranean group centred in southwestern Turkey and extending in area from the Caucasus to Macaronesia, north to Scotland, Denmark and southern Sweden, east to Belarus and the Ukraine and south to north-west Africa and Israel. Section 15. Thasia has been included in Section 16. Crossophyllum. Two new species are described in Section 12. Origanifolium (H. laxiflorum N. Robson, sp. nov. and H. ichelense N. Robson, sp. nov.) and five changes of rank are made; in Section 10. Olympia: H. lycium( N. Robson & Hub.-Mor.) N. Robson, stat. nov. and H. auriculatum (N. Robson & Hub.-Mor.) N.Robson, stat. et nom. nov.; in Section 12. Origanifolia: H. origanifolium var. depilatum (Freyn & Bornm.) N. Robson, stat. nov., H. bourgaei (Boiss.) N. Robson, stat. nov. and H. albiflorum (Hub.-Mor.) N. Robson, stat. nov. In addition, in Section 14. Oligostema, Druce's name for the hybrid H. linariifolium x humifusum has been validated (H. x caesariense Druce ex N. Robson, hybr. nov.); and H. leprosiforme O.Schwartz has been moved from Section 12. Origanifolia to Section 27. Adenosepalum.
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Part 5(2) of this monographic series of papers on the genus Hypericum contains treatments of the remaining sections: Sections 17. Hirtella, 18. Taeniocarpium and 19. Coridium, which form a related group centred in eastern Turkey and Transcaucasia and extending in area from Morocco, Portugal and Ireland to western Xinjiang and the Altai and southern Angara-Sayan regions of Siberia. One new series, one new species and one new subspecies are described in Section 17. Hirtella (Series Scabra N.Robson, ser. nov., H. hedgei N.Robson, sp. nov., H. hyssopifolium subsp. acutum N.Robson, subsp. nov.), and two new species and one new subspecies in Section 18. Taeniocarpium (H. pseudorepens N.Robson, sp. nov., H. vaccinioides N.Robson, sp. nov., H. armenum subsp. iranicum N.Robson, subsp. nov.). Four new combinations or changes of rank are made, three in Section 17 (H. elongatum var. lythrifolium (Boiss.) N.Robson, comb. nov., H. elongatum var. racemosum (Kuntze) N.Robson, comb. nov., H. elongatum var. antasiaticum (Grossh.) N.Robson, stat. nov.) and one in Section 18: H. linarioides subsp. alpestre (Steven) N.Robson, stat. et comb. nov.