Molecular phylogeny of Acanthophyllum (Caryophyllaceae: Caryophylleae), with emphasis on infrageneric classification

Abstract

Despite being one of the larger genera of Caryophyllaceae with about 60 cushion-forming subshrubby species, Acanthophyllum is represented poorly in previous molecular phylogenetic studies. The genus is an important component of the subalpine steppe flora in Central to Southwest Asia. Although the placement of Acanthophyllum in the tribe Caryophylleae and a close relationship to Allochrusa has already been suggested, the monophyly of the genus and its infrageneric taxa, as well as its relation to other closely related genera, have not been addressed. We have assembled datasets of nuclear ribosomal internal transcribed spacer (ITS) sequences and intron sequences of the chloroplast gene rps16 for 47 Acanthophyllum species and 63 species of 11 additional genera from Caryophylleae. Phylogenetic analyses were performed using maximum parsimony, maximum likelihood and Bayesian methods. Our analysis suggests that Allochrusa, Diaphanoptera, Ochotonophila and Scleranthopsis are nested within Acanthophyllum but that the traditionally recognized sections of Acanthophyllum are monophyletic after reassignment of a few species. Emarginate petals may be a synapomorphy for one of the two basal clades of Acanthophyllum. Moreover, non-monophyly of the genera Gypsophila and Diaphanoptera is suggested by the present study. The age of the crown clade of Acanthophyllum s.l. is estimated to be 11.1 Ma by *BEAST species tree analysis.

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
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• Molecular phylogeny of Acanthophyllum
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 
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INTRODUCTION
Acanthophyllum     




        

Acanthophyllum     





Acanthophyllum 

   

  Acanthophyl-
lum   


 Acanthophyllum    
 
 

Flora Iranica 
    Flora of the
U.S.S.R.Flora of Uzbekistan    
Flora of Tajikistan
             
  
 

 
Acanthophyllum 
   Acantho-
phyllum      


  

Allochrusa . 
 Euacantho-
phyllum  Allochrusa  
Allochrusa 
PseudacanthophyllumGyp-
sophilaAcanthophyllum   Scapif lora
Molecular phylogeny of Acanthophyllum (Caryophyllaceae:
Caryophylleae), with emphasis on infrageneric classification
Atefeh Pirani,1,2 Shahin Zarre,1 Bernard E. Pfeil,2 Yann J.K. Bertrand,2 Mostafa Assadi3 & Bengt Oxelman2
 Depart ment of Plant Biolog y, and Center of Excellence in Phylogeny of Living Organisms, School of Biology, College of Science,

  
 
 Atefeh Pirani, pirani@khayam.ut.ac.ir; Shahin Zarre, zarre@khayam.ut.ac.ir
DOI

Abstract
    
Acanthophyllum   
Acanthophyllum     
 Allochrusa 

 Acanthophyllum 

Allochrusa Diaphanoptera Ochotonophila Scler-
anthopsis    Acanthophyllum             Acanthophyllum     
Acanthophyl-
lum.Gypsophila Diaphanoptera 
Acanthophyllum 
Keywords
Acanthophyllum



• Molecular phylogeny of Acanthophyllum
TAX ON

Version of Record (identical to print version).
AcanthophyllumScapi-
flora
Gypsophila  Saponaria
 Acanthophyllum  


Acanthophyllum 
 
Acanthophyllum

Fig. 1 (in two parts).

A–B,
     Acanthophyllum
C–E,
A. speciosum    Oligosperma
F–G,
A. gracile    Macrostegia
H,
A. bracteatum    Macrostegia
I–K,
A. crassifolium    Acanthophyllum
L–M,
A. glandulosum    Pleiosperma
N,
A. spinosum
  Pleiosperma
O–P,
A. caespitosum   Oligosperma


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

• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
Macrodonta


 


    


 

AAcanthophyllumMacrostegia 
Oligosperma Pleiosperma

    
Acantho-
phyllum 
 Acantho-
phyllum, Gypsophila SaponariaDianthus
Scler-
anthopsis AllochrusaOchotonophila Diapha-
noptera Kuhitangia 



• Molecular phylogeny of Acanthophyllum
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
Version of Record (identical to print version).
Acanthophyllum      
   
 matK
Allochrusa versicolor Acanthophyl-
lum sordidum
Acanthophyllum
Allochrusa    
All. versicolorA. sordidum  
A. paniculatum    
Allo-
chrusa  A. sordidumAcanthophyl
-
lum  
.
Acantho-
phyllumAcanthophyllumAllochrusa
      

Allochrusa Acanthophyllum


        
Acanthophyllum     

Acanthophyllum


   Acanthophyllum
Acanthophyllum 

Table 1.
Acanthophyllum
 

 

Euacanthophyllum
a

Allochrusa


Macrodonta

Macrodonta
—
Macrodonta

A. grandiflorum


Macrostegia

Macrostegia
.

Macrostegia
.
—
Macrostegia

A. bracteatum
.

Turbinaria

Turbinaria 

Turbinaria

—
Acanthophyllum
A. mucronatum


Pleiosperma

Pleiosperma


Pleiosperma

—
Pleiosperma

A. spinosum


Euacanthophylla

Euacanthophylla

Oligosperma

—
Oligosperma

A. squarrosum

———— Pseudacantho phyllum

Gypsophila
Pseud acanthophyllum
A. laxiflorum

————
Scapiflora

A. scapiflorum

———
Versicoloria

A. versicolor

—
Paniculata

—
Paniculata

A. paniculatum

aAcanthophyllum

TurbinariaAcanthophyllum
EuacAcanthophyllum A. mucronatum 
Turbinaria.


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

• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
MATERIALS AND METHODS
Sampling st rategy and plant material. —
   

Acanthophyllum   
Silene            




 Acanthophyllum
 Diaphanoptera Allochrusa Ochotonophila
Scleranthopsis GypsophilaAcantho-
phyllum     
 
 
A. lilacinum D. afghanica 
A. paniculatum 
  
 Gypsophila 
SaponariaDianthusPetrorhagiaVele z ia 
Psammosilene  Vaccaria  Bolbo-
saponariaSilene

           

 
       

DNA extraction, PCR, and sequencing. —
 
         


   

    

   
  
   

 
      

  
   

Sequence assembly, alignment and analysis. —



    
  




  

  





Fig. 2.
A,
 

B,


C,

D,

E,

F,

G
 
H,






• Molecular phylogeny of Acanthophyllum
TAX ON

Fig. 3.
* Acanthophyllum 

CLADE II
QUATERNARY
PLIOCENE
MIOCENE
Sect. Acanthophyllum
Sect. Oligosperma
Sect. Scapiflora
Sect. Pseudacanthophyllum
Clade E
Clade C
Clade G
Clade H
Clade F
Clade K
Clade J
Clade A
Clade D
0.84
0.81
0.74
0.63
0.83
0.98
0.7
0.92
0.97
0.54
0.61
0.46
0.77
0.99
0.56
0.51
0.88
0.96
0.99
0.71
0.5
0.76
0.96
0.66
0.82
0.93
0.99
0.91
0.94
2.5
5
7.5
10
12.5
Poorly branched inflorescence
A. leucostegium
Clade L
Emarginate petals
Solitary flowers
Membranous bracts
Ovules ≥ 8
Ochotonophila allochrusoides
A. pleiostegium
A. schugnanicum
A. glandulosum
A. crassinodum
A. spinosum
A. kandaharicum
A. longicalyx
Diaphanoptera lindbergii
Diaphanoptera stenocalycina
A. gracile
A. bracteatum
A. pachycephalum
A. heratense
A. pachystegium
A. andarabicum
A. borsczowii
A. squarrosum
A. ejtehadii
A. diezianum
A. speciosum
A. heterophyllum
A. laxiusculum
A. yasamin-nassehiae
A. kabulicum
A. stocksianum
A. andersenii
A. adenophorum
A. subglabrum
A. macrodon
A. korshinskyi
A. grandiflorum
A. xanthoporphyranthum
A. anisocladum
A. raphiophyllum
Scleranthopsis aphanantha
A. laxiflorum
A. scapiflorum
A. stewartii
A. sordidum
A. kurdicum
Diaphanoptera ekbergii
A. verticillatum
A. acerosum
A. mucronatum
A. microcephalum
Allochrusa versicolor
Allochrusa bungei
A. crassifolium
A. oppositiflorum
A. caespitosum
0
Sect. Pleiosperma
Sect. Macrodonta
Sect. Macrostegia
Sect. Macrodonta
Sect. Scapiflora
Sect. Oligosperma
Sect. Acanthophyllum
Sect. Pleiosperma
6x; ovules 8–12(–16)
2x; ovules 4
2x; ovules 4
4x; ovules (6–)8(–10)
4x; ovules 4–8
2x; ovules 4
CLADE I
Clade B


TAX ON


• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
   
t

   



  
  

    

  


      

 
            

Species tr ee inference and dating . —
     


   Gypsophila cerastioi-
des  
  
  

         
    



  
  


  
     
  

     



    
    


                 






RES U LT S
Species tree inference and dating. —

Acanthophyllum 


 
A.Pseudacanthophyllum Scapif lora
 Diaphanoptera ekbergii   
 A.
Macrodonta Macrostegia  Pleiosperma 
OligospermaOchotonophila allochrusoides
Scleranthopsis aphanantha Diaphanoptera
stenocalycina  D. lindbergii
A  Acantho-
phyllumA. pleiostegium
 A
Acanthophyllum Allochrusa bungei   All. versi-
color  
Acanthophyllum sordidumAPleiosperma
A. caespi tosum A. Oligosperma 

    Acanthophyllum

          
         

Phylogenetic analyses. —

    

  
     


         

Table 2.


 rps16
  
  
  
  
  
  
  
  
  
  
  



• Molecular phylogeny of Acanthophyllum
TAX ON


    
Acanthophyllum 

Ochotono-
philaScleranthopsisDiaphanoptera  
GypsophilaAcanthophyllum
 Allochrusa Acanthophyllum
Acantho-
phyllum     
A.Oligosperma Pleiosperma 
Scapiflora Pseudacanthophyllum Macrostegia 
Macrodonta 
Diaphanoptera Ochotonophila Scleranthopsis 
Gypsophila. A.Oligosperma
Fig. 4.
      

1
1
98
100
1
1
1
1
1
1
99
100
100
1
99
1
87
1
71
100
1
1
1
89
100
0.86
1
91
1
91
1
68
1
100
1
100
1
89
1
84
1
100
1
0.66
72
1
1
100
1
1
1
Saponaria
Vaccaria hispanica
Bolbosaponaria bucharica
Diaphanoptera afghanica
Velezia rigida
Gypsophila muralis
Gypsophila cerastioides
Diaphanoptera ekbergii
A. scapiflorum
A. anisocladum
A. laxiflorum
A. stewartii
A. raphiophyllum
A. stocksianum
A. subglabrum
A. andersenii
A. squarrosum
A. heterophyllum
A. borsczowii
A. pachystegium
A. lilacinum
A. heratense
A. speciosum
A. diezianum
A. yasamin-nassehiae
A. kabulicum
A. laxiusculum
A. ejtehadii
A. korshinskyi
A. adenophorum
A. andarabicum
A. bracteatum
A. leucostegium
A. kandaharicum
A. gracile
A. paniculatum
Diaphanoptera lindbergii
Diaphanoptera stenocalycina
A. longicalyx
A. schugnanicum
A. crassinodum
A. glandulosum
A. spinosum
A. pleiostegium
Ochotonophila allochrusoides
Scleranthopsis aphanantha
A. xanthoporphyranthum
A. macrodon
A. grandiflorum
A. oppositiflorum
A. acerosum
A. crassifolium
A. verticillatum
A. mucronatum
A. caespitosum
A. kurdicum
A. microcephalum
A. sordidum
Allochrusa versicolor
Allochrusa bungei
Psammosilene tunicoides
Petrorhagia
Dianthus
Gypsophila
Gypsophila
Silene
1
86
0.94
1
98
1
53
Clade I
Acanthophyllum s.l.
Clade II
Sect. Acanthophyllum
Sect. Macrodonta
Sect. Pleiosperma
Sect. Macrostegia
Sect. Oligosperma
Sect. Macrodonta
Sect. Paniculata
Sect. Scapiflora
Sect. Pseudacanthophyllum
Sect. Acanthophyllum
Sect. Acanthophyllum
Sect. Oligosperma
Sect. Pleiosperma
A. pachycephalum


TAX ON


• Molecular phylogeny of Acanthophyllum

Macrodonta Macrostegia 
 A
Acanthophyllum A. pleiostegiumA. sor-
didum    Pleiosperma A. caespitosum    Oligo-
spermaAllochrusa 
   

DISCUSSION
Phylogenetic position of Acanthophyllum within tribe
Caryophylleae. —
Acanthophyllum
 

  
Fig. 5.


  





1
100
1
97
0.68
54
0.99
60
0.9
63
1
87
0.85
0.94
1
79
1
93
64
1
79
1
93
1
95
0.97
66
1
86
0.94
1
95
0.96
72
1
100
1
100
1
93
1
100
1
90
1
100
1
1
100
Clade I
Silene
Petrorhagia saxifraga
Dianthus
Gypsophila cerastioides
Diaphanoptera ekbergii
A. raphiophyllum
A. stewartii
A. anisocladum
A. laxiflorum
A. scapiflorum
Ochotonophila allochrusoides
A. pleiostegium
A. spinosum
A. schugnanicum
A. crassinodum
A. glandulosum
Diaphanoptera lindbergii
Diaphanoptera stenocalycina
A. longicalxy
A. heratense
A. squarrosum
A. kabulicum
A. pachystegium
A. heterophyllum
A. subglabrum
A. korshinskyi
A. yasamin-nassehiae
A. laxiusculum
A. borsczowii
A. ejtehadii
A. speciosum
A. andersenii
A. adenophorum
A. stocksianum
A. diezianum
A. gracile
A. kandaharicum
A. pachycephalum
A. bracteatum
A.leucostegium
A. macrodon
A. grandiflorum
A. xanthoporphyranthum
Scleranthopsis aphanantha
A. andarabicum
A. oppositiflorum
A. crassifolium
A. kurdicum
A. acerosum
A. verticillatum
A. mucronatum
A. microcephalum
Allochrusa versicolor
Allochrusa bungei
A. sordidum
A. caespitosum
Gypsophila paniculata
Saponaria
Acanthophyllum s.l.
Sect. Pseudacanthophyllum
Sect. Scapiflora
Sect. Pseudacanthophyllum
Sect. Scapiflora
Sect. Acanthophyllum
Sect. Pleiosperma
Sect. Macrodonta
Sect. Oligosperma
Sect. Macrostegia
Sect. Macrodonta
Sect. Acanthophyllum
Sect. Pleiosperma
Sect. Oligosperma
Clade II
100 0.98



• Molecular phylogeny of Acanthophyllum
TAX ON

Version of Record (identical to print version).

AcanthophyllumScleranthopsis Ochotonophila 
Diaphanoptera 
  Acanthophyllum  
  
 Acanthophyllum  Acanthophyl-
lumScleranthopsis AllochrusaOchotonophila Diaphanop-
tera   
 Acan-
thophyllum  Allochrusa Scleranthopsis Ochotonophila
Diaphanoptera  



Acanthophyllum
Acan-
thophyllum  Allochrusa Ochotonophila
Diaphanoptera Scleranthopsis
DianthusPetrorhagia  Vele -
zia 

Gypsophila
cerastioidesAcanthophyllum 
G. muralisDianthus-
Petrorhagia 

Circumscription of Acanthophyllum. —
   
Acanthophyllum 
  
 Acanthophyllum 
Acantho-
phyllum 
Scleranthopsis. —
  Scleranthopsis 


Acanthophyllum aphanan-
thum       Aphanantha

Scleranthopsis 
   
 .
Scleranthopsis Acantho-
phyllum Aphanantha
Allochrusa. —
Allochrusa 
 

 Acanthophyllum     
Acanthophyl-
lum        
Allochrusa 
Allochrusa  
VersicoloriaPaniculata

  
. Allochrusa 
   

Allochrusa versicolor  All. bungei    
 Acanthophyllum 


 
Allochrusa Acantho-
phyllum   


Allochrusa bungei  All. versicolor
Allochrusa  .    Acantophyl
-
lum paniculatumAllochrusa
Paniculata    Allochrusa
   Acanthophyllum paniculatum


All. versicolor bungei 

Acanthophyllum    

A. paniculatum 

               
Allochrusa Acanthophyllum 
Ochotonophila. —
Ochotonophila    

       


O. allochrusoides 
 Acantho phyllum Gypsophila
O. eglandulosa 

Acanthophyllum Gypso phila.  
Ochotonophila
Acanthophyllum Scleranthopsis 
Allochrusa.             
Ochotono philaAllochrusa Scleranthopsis
Acanthophyllum Gypso phila.Ochotonophila 
 Acanthophyllum         
Ochotonophila allochrusoides
A. Pleiosperma A. pleiostegium A 
AcanthophyllumA. longicalyxA 
Macrodonta      . 
Ochotonophila A.Pleiosperma
Ochotonophila
Acanthopyllum 
Diaphanoptera. —
Diaphanoptera  
          
   
         
       D. khorassanica
Acanthophyllum 
       
    
   
 Diaphanoptera Acan-
thophyllumDiaphanoptera afghanica


TAX ON


• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
Bolbosaponaria 
Gypsophila Diaphanop-
tera stenocalycina D. lindbergii D. ekbergii  
Acanthophyllum  Diaphanop-
tera lindbergii D. stenocalycina   
  
 
  
 D. ekbergii
A.  Pseudacanthophyllum Scapif lora
 
 
 Gypsophila cerastioides
 
D. khorassanica 
Diaphanoptera  Acanthophyllum Gypsophila
Ochotonophila 
Diaphanoptera

Gypsophila. —
Gypsophila 
   

AcanthophyllumGypsophila 

 

      


Acanthophyllum Pseudacanthophyllum
Gypsophila Acantho-
phyllum          
. 
Acanthophyllum

 G. cerasti-
oides  Acanthophyullum  Gypsophila muralis
DianthusPetrorhagia
  
 Gypsophila 
 Gypsophila  

 G. cerastioidesGypsophila
  Acanthophyllum  
Gypsophila 

Infrageneric classification of Acanthophyllum s. st r. —
 
 
Acanthophyllum  Pseudacanthophyllum Scapi-
flora 
AcanthophyllumMacrostegia
     Acanthophyllum
Pleiosperma    
Oligosperma 

Acanthophyllum Macrodonta
A. longicalyx
AAcanthophyllum      

A.Oligosperma  A. 
Acanthophyllum
 
   
      

  
   
      





A. pleiostegium
O. allochrusoides

 

Clade I. —
AcanthophyllumScapif lora Pseud-
acanthophyllum Macrodonta  Pleiosperma 
MacrostegiaOligosperma 
Acanthophyllum Scapiflora Macrodonta
A. 
Acanthophyllum A. pleiostegium     
Acanthophyllum  Scapiflora Pseudacanthophyl-
lum Macrodonta Pleiosperma Macrostegia
Oligosperma

   

 

Clade A. –   APseud-
acanthophyllum Scapif lora D. ekbergii 
 Acanthophyllum
 
  A. laxiflorum 



Acanthophyllum anisocladum A. sca-
pi florum  Scapiflora 
A. laxif lorum A. raphiophyllum   
A.Pseud-
acanthophyllum      
  
  
AScapif lora 
APseudacanthophyllum 

   

 




• Molecular phylogeny of Acanthophyllum
TAX ON

Version of Record (identical to print version).
Clade B. –      A.  Macro-
donta  Pleiosperma  Macro stegia
Oligosperma 
A. AcanthophyllumDiaphanopteraOchotono-
philaScleranthopsis

Clade D. –
      
AMacrodonta A. longicalyx
    Acanthophyllum
longicalyx 
     

Macrodonta
.
Clade E. –Ochotonophila
allochrusoidesAPleiosperma    Asordidum
Apleiostegium    Acanthophyllum Alongicalyx    
Macrodonta Diaphanoptera lindbergii  D. stenoca-
lycina  A. pleiostegium    

O. allochrusoides
Clade H. –A.
Macrostegia. 
 
    

Acanthophyllum sect. Oligosperma. —


A. Oligosperma   
 Acaespitosum  
A. andarabicum  
    
     

AOligosperma 
 Elatiora A. elatius 
   

A. elatius Oligosperma.

A.Oligosperma  
 
Clade II. —
   
 
A Acanthophyllum   
 
A. acerosum .
  
A. oppositif lorum    
A. acerosum A. verticillatum  A. mucronatum
   A. microcephalum A. kurdicum
A. crassifolium Acantophyllum
oppositif lorum   

 A.  Acantophyllum

Acanthophyllum Acanthophyllum   
 

A. pleiostegium Acanthophyllum 

Acanthophyllum caespitosum   Oligosperma 
A. sordidum     Pleiosperma     
  
Acanthophyllum caespitosum A.
Oligosperma    

 A Oligosperma
A. caespitosum  
Acantophyllum   
x   x 

A. caespitosum 
A. caespitosumA.Oligosperma

   A.  Acanthophyllum
A. caespitosumA.Acanthophyllum

    Acantho-
phyllum  A. caespi-
tosum
 
A. caespitosum AAcanthophyllum
Acanthophyllum sordidum     A
Pleiosperma     
   


   A. sordidum 
A.Pleiosperma
A. sordidum 
A Acanthophyllum
A.  Pleiosperma .
 
A. sordidum AAcanthophyllum.  
A. sordidum  A.
Pleiosperma

Acanthophyllum
 
     
Acanthophyllum
    
  


.   

A. aphananthum
ScleranthopsisO. allochrusoides 
 OchotonophilaApachycephalum
A. pleiostegiumA. sordidumA. oppositif lorum    


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

• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
AcanthophyllumMacrostegia 
Oligosperma 
          
A.Acanthophyllum  
A.Pleiosperma    
 Acanthophyllum    
 AcanthophyllumAcanthophyllum



    A. pungens
 Oligosperma
Acanthophyllum Oligosperma     


Acanthophyllum Oligosperma 
Acanthophyllum    

  Acanthophyllum  
  AScapifloraOchotonophila
Aphanantha
Divergence time of Acanthophyllum. —
  

Acanthophyllum-Allochrusa    
matK
 Acan-
thophyllum AllochrusaA. sordidum  All. versicolor
  Allo chrusa
AcanthophyllumA. sordidum All.
versicolor  All.bungei   
A. sordidumAllochrusa

A. sor-
didumAllochrusa     
  

Allochrusa
Acanthophyllum 
matK.
Acantho-
phyllum     
  

      





TAXONOMIC IMPLICATIONS
Acanthophyllum   
A. mucronatum
Ochotonophila     
syn. nov. O. allochrusoides
Allochrusa
AcanthophyllumAllochrusa
    
All. versicolor
New names and combinations
Acanthophyllum  Ochotonophila comb.
& stat. nov.Ochotonophila      
 A. allochrusoides

      
   

Acanthophyllum allochrusoides   comb. nov.
 Ochotonophila allochrusoides     
    

  
Acanthophyllum eglandulosum 
comb. nov.  Ochotonophilaeglandulosa  
  
   
Hedge &

Section to be reinstated
AcanthophyllumAphanantha        
Scleranthopsis 
 Acathophyllum aphananthum

ACKNOWLEDGEMENTS



                    
      
   
  

                
Acanthophyllum     
                  

                 
                 

           





• Molecular phylogeny of Acanthophyllum
TAX ON

Version of Record (identical to print version).
LITERATURE CITED
Aghel, N., Moghimipour, E. & Raies Dana, A. 
Acanthophyllum squar-
rosumIran. J. Pharm. Res. 
Amini, E., Zarre, S. & Assadi, M. 
  Gypsophila
Nordic J. Bot. 
 
Aytaç, Z. Acanthophyllum 
Nordic J. Bot. 
   
Barkoudah, Y.I. GypsophilaBolanthusAnk yro-
petalumPhr ynaWen tia
Basiri-Esfahani, Sh., Bidi, B., Assadi, M. & Rahimi-Nejad, M.R.
Acanthophyllum  
Iran. J. Bot.
Bentham, G. & Hooker, W.J. Genera plantarum .
 
Bittrich, V.  
The families and genera of vascular plants
Boissier, E.    Flora orientalis
 
Drummond, A.J. & Rambaut, A.        
B. M. C. Evol. Biol
 
Drummond, A.J., Ho, S.Y.W., Phillips, M. J. & Rambaut, A. 
PLoS Biol.

Eggens, F., Popp, M., Nepokroeff, M., Wagner, W. L. & Oxelman, B.

SileneAmer. J. Bot. 
 
Fior, S., Karis, P.O., Casazza, G., Minuto, L. & Sala, F. 
                
matK        . Amer. J.
Bot.
Frajman, B., Eggens, F. & Oxelman, B. 
     Heliosperma 

Syst. Biol
   
Gaidi, Gh., Miyamoto, T., Rustaiyan, A., Laurens, V. & Lacaille-
Dubois, M.A.    
Acanthophyllum squarrosum. J. Nat. Prod. (Lloydia) 

Gaidi, Gh., Miyamoto, T., Rustaiyan, A. & Lacaille-Dubois, M.A.
Acanthophyl-
lum glandlosum. J. Nat. Prod. (Lloydia) 
 
Gaut, B.S., Morton, B.R., McCaig, B.C. & Clegg, M.T. 

 Adh  
rbcLProc. Natl. Acad. Sci. U.S.A.

Ghaffari, S.M.   
Acanthophyllum  J.
Sci. Univ. Tehran
Ghaffari, S.M. Biosystematic study of some 
species
Ghaffari, S.M.  Acanthophyl-
lum   Biologia (Bratislava) 
Ghazanfar, S.A. & Nasir, Y.J. Acanthophyllum. 
Flora of Pakistan

Gilli, A.              Feddes Repert.
Spec. Nov. Regni Veg.
Gilli, A.  Gypsophila Acan-
thophyllum. Oesterr. Bot. Z 
  
Golenkin, M. AcanthophyllumTrudy Imp.
S.-Peterburgsk. Bot. Sada
Greenberg, A.K. & Donoghue, M.J. 
Tax on  
Harbaugh, D.T., Nepokroeff, M., Rabeler, R.K., McNeill, J.,
Zimmer, E.A. & Wagner, W.L. 
 Int. J. Pl. Sci. 
  
Hedge, I. & Wendelbo, P.  
Aarbok Univ. Bergen, Mat.-Naturvitensk. Ser.
Heled, J. & Drummond, A.J.           
Molec. Biol. Evol. 
   
Huang, Y., Liu, Y., Jacques, F.M.B., Su, T., Xing, Y. & Zhou, Z.
Cucubalus
   Rev. Palaeobot.
Palynol. 
  
Huelsenbeck, J.P. & Ronquist , F. 
Bioinformatics
   
Jordan, G.J. & Macphail, M.K. 
 Amer. J.
Bot.
Kay, K.M., Whittal l J.B. & Hodges S.A. 
   
       
B. M. C. Evol. Biol. 
  
Kool, A., Perrigo, A. & Thulin, M. 
Sphaerocoma 
Taxo n
Kurtto, A.                Flora
Nordica Chenopodiaceae to Fumariaceae

Laínz, M. & Garmendia, F.M.  
Castroviejo, S., Laínz, M., González, G.L., Montserrat, P.,
Garmendia, F.M., Paiva, J. & Vil lar, L. (eds.)Flora iberica:
Plantas vasculares de la Península Ibérica e Islas Baleares

Lewis, P.O. 
Syst. Biol. 
   
Mahmoudi-Shamsabad, M., Vaezi, J., Memariani, F. & Joharchi,
M.R.    Acanthophyllum
 Iran. J. Bot.

Meyer, C.A. von -
   
   

Miller, M.A., Pfeiffer, W. & Schwartz, T. 
     
Workshop
  
Müller, K. 
Appl. Bioinf. 
Oliver, D.J.   
 .
Trans. Linn. Soc. London
 
Ovchinnikov, P.N. Acanthophyllum         
 Flora Tadzhikskoi SSR   



TAX ON


• Molecular phylogeny of Acanthophyllum
Version of Record (identical to print version).
Oxelman, B. & Lidén, M. 
                  
Taxo n
Oxelman, B., Lidén, M. & Berglund, D. 
Pl. Syst. Evol.
   
Oxelman, B., Lidén, M., Rabeler, R.K. & Popp, M. 
 Nor-
dic J. Bot

Petri, A. & Oxelman, B. Silene
PhysolychnisTax on
Pirani, A., Joharchi, M.R. & Memar iani, F.  
Acanthophyllum   Phytotaxa 

Popp, M. & Oxelman, B. 
Silene aegaea 
Molec. Phylogen. Evol. 
 
Popp, M., Eggens, F., Erixon, P. & Oxelman, B.   
Silene 

Syst. Bot. 
 
Popp, M. & Oxelman, B.           
SileneAmer. J. Bot
 
Posada, D.    Molec.
Biol. Evol. 
Rambaut, A. 

Rambaut, A. & Drummond, A.J. 

Rautenberg, A., Hauthaway, L., Oxelman, B. & Prentice, H.C.
         Silene  
Melandrium  
Molec. Phylogen. Evol
     
Rechinger, K.H.  
  
Repert. Spec. Nov.
Regni Veg. 
Rechinger, K.H. Oesterr.
Bot. Z
Rechinger, K.H.    Scleranthopsis  
Ann. Naturhist. Mus. Wien
Schiman-Czeika, H.       
Acanthophyllum  Pl. Syst.
Evol
Schiman-Czeika, H. Acanthophyllum
Flora Iranica

Schischk in, B.K. Acanthophyllum

         
Flora of the U.S.S.R.  



Simmons, M.P. & Ochotorena, H.     
Syst. Biol. 
 
Sparg, S.G., Light, M.E. & van Staden, J. 
J. Ethnopharmacol. 
      
Sukumaran, J. & Holder, M.T.  

Bioinformatics

   
Swofford, D.L. 
                 

Takhtajan, A.   
     
Valente, L.M., Savolainen, V. & Vargas, P.     
Proc. Roy. Soc. London, Ser. B,
Biol. Sci. 
Vvedensky, A.I. Acanthohpyllum
 Flora of Uzbekistan

Williams, F.N.   GypsophilaJ. Bot. 

Wolfe, K.H., Li, W.H. & Sharp, P.M. 

Proc. Natl. Acad. Sci. U.S.A.
 
Yue, J.X., Li, J., Wang, D., Araki, H., Tian, D. & Yang, S. 
    
B. M. C. Pl. Biol.
    
Yukhananov, D.KH.   Acantho-
phyllum  Allochrusa  
& Leningrad)  
Zakirov, K.Z. & Musaeva, M. Acanthophyl-
lumUzbeksk. Biol. Zhurn. 
Zohary, M. Geobotanical foundations of the Middle East

Appendix 1.
 collector(s)voucher r ps16

Acanthophyllum acerosum   Zarre & al. 41900     Acanthophyllum adenophorum 
Pirani & Moa zzeni 1947           Acanthophyllum andarabicum   
  Acanthophyllum andersenii   Anders & Peterson 320
   Acanthophyllum anisocladum       Acanthophyl-
lum borsczowiiZarre & al. 41034  Acanthophyllum bracteatum
Pirani & Moazzeni 2104      Acanthophyllum caespitosum  Zarre & al. 41903
 Acanthophyllum crassifolium        Pirani & Moazzeni 41702 Acanthophyl-
lum cras sinodum            Pirani & Moazzeni 2923   Acanthophyllum diezianum
Zarre & al. 41040   Acanthophyllum ejtehadii Pirani & Moazzeni
2181   Acanthophyllum glandulosum          Zarre & al. 41037 
Acanthophyllum gracile       Pirani & Moazzeni 2989       Acanthophyllum grandiflorum
Podlech 1340   Acanthophyllum heratensePirani & Moa zzeni 2152
     Acanthophyllum heterophyllum Pirani & Moazzeni 2921   
Acanthophyllum kabulicumFrey s.n.   Acanthophyllum kandaharicum
Joharchi & Zangouei 36245    Acanthophyllum korshinskyi Pirani & Moazzeni
2123          Acanthophyllum kurdicum   Hamzehee & Lashkarbolooki 1756  
 Acanthophyllum laxiflorum      Ekberg W918 4     Acanthophyllum



• Molecular phylogeny of Acanthophyllum
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
Version of Record (identical to print version).
laxiusculum          Pirani & Moazzeni 1941     Acanthophyllum leucostegium        
Ghahreman & Mozaffarian 5656    Acanthophyllum lilacinumPodlech &
Ja rm al 29855  Acanthophyllum longicalyx   Freitag 6580   
Acanthophyllum macrodonHedge & al. W7641 Acanthophyllum microcephalum
Rajamand & Bazargan 32055     Acanthophyllum mucronatumAssadi & Olfat
68668   Acanthophyllum oppositiflorumAy ta ç 7476  Acanthophyl-
lum paniculatum Acanthophyllum pachycephalum Ganjalizadeh 6106
Acanthophyllum pachystegium        Hedge & Wendelbo W9282  Acanthophyllum
pleiostegium       Acanthophyllum raphiophyllum
  Podlech 12548          Acanthophyllum scapiflorum  
Podle ch 31232Acanthophyllum schugnanicumWendelbo & Ekberg W9796
    Acanthophyllum sordidumPirani & Moazzeni 2147   Acantho-
phyllum speciosum   Pirani & Moazzeni 2186   Acanthophyllum spinosum
 Pirani & Moazzeni 2150 Acanthophyllum squarrosum  Pirani & Moazzeni
2974            Acanthophyllum stewartii  Anders 8994  
   Acanthophyllum stocksianumTonc ev s. n .            Acanthophyllum
subglabrum Hedge & al. W7483  Acanthophyllum verticillatum 
Mozaffarian & Sardabi 42175    Acanthophyllum xanthoporphyranthum
Hedge & al. W8003Acanthophyllum yasamin-nassehiae Memariani & Zangouei 41448
     Allochrusa bungei  Rechinger 43834 Allochrusa versicolor
Nydegger 43597b    Bolbosaponaria bucharica  Dianthus anatolicus
Dianthus armeriaDianthus capitatusDianthus carthusianorumDi-
anthus charidemiDianthus ciliatusDianthus corymbosus Dianthus costae
Dianthus crassipes  Dianthus crinitus    Dianthus cyri     Dianthus
diffususDianthus erinaceusDianthus gracilisDianthus hyssopifoliusDian-
thus laricifolius Dianthus microlepisDianthus micropetalusDianthus orientalis
 Dianthus pyrenaicus  Dianthus serratifolius Dianthus thunbergii
  Dianthus turkestanicus  Dianthus versicolor Diaphanoptera afghanica 
Po dl ech 21075  Diaphanoptera ekbergii  Po d le c h 1184 8 
1176 0      Diaphanoptera lindbergii        Hedge & al. W8336  
Diaphanoptera stenocalycinaAttar & Mehdigholi 24422   Gypsophila arrostii
Gypsophila aucheri  Gypsophila bicolor     Gypsophila capituliflora   Gypso-
phila cephalotesGypsophila cerastioides
Gypsophila curvifoliaGypsophila desertorum  Gypsophila elegans Gypsophila fastigiata
Gypsophila heteropoda    Gypsophila montserratii       Gypsophila muralis   Gypso phila
paniculataGypsophila patriniiGypsophila pilulifera Gypsophila pinifolia
Gypsophila scorzonerifoliaGypsophila silenoides Gypsophila steveni 
 Gypsophila violacea  Ochotonophila allochrusoidesWendelbo & Ekberg W9801 
      Petrorhagia prolifera   Petrorhagia saxifrage  Petrorhagia thessala
Petrorhagia velutina    Psammosilene tunicoides 
Saponaria ocymoidesSaponaria officinalis Saponaria pumilaScler-
anthopsis aphananthaRechinger 31265  Silene ampullataSilene
austroiranica         Silene campanulata    Silene cariensisSilene
conoideaSilene corinthiacaSilene dioica  Silene echinosperma 
Silene fruticosaSilene latifoliaSilene martyiSilene men-
tagensis     Silene nana   Silene nutans Silene reticulata       
Silene vulgarisVaccaria hispanicaVelezia rigida
Appendix 1.
