Generic phylogeny and character evolution in Urticeae (Urticaceae) inferred from nuclear and plastid DNA regions

Abstract

This study examines phylogenetic relationships among the 12 genera of Urticeae (Urticaceae) and investigates the pattern of morphological evolution based on analysis of nuclear ribosomal internal transcribed spacer (nrITS) and two plastid DNA regions (rbcL exon, trnL-F spacer). Sequence data were analyzed using maximum parsimony and Bayesian inference, and selected morphological traits were mapped onto the molecular tree. The molecular results strongly supported monophyly of Urticeae, excluding Gyrotaenia, which is related to Elatostemateae. All genera were monophyletic except for Urtica, Laportea, and Urera. Two Hesperocnide species are nested within Urtica. Laportea and Urera are divided into three groups with a strong geographical signal. The inferred phylogeny indicates five well-supported clades in Urticeae: clade A including Urtica (with
Hesperocnide), Zhengyia, Laportea I, and Nanocnide; clade B comprising Dendrocnide and Discocnide; clade C including only Girardinia; clade D including Laportea II; and clade E including Obetia, Urera I, II, III, and Poikilospermum. Although it is difficult to identify morphological synapomorphies for these well-defined clades within Urticeae, character analysis shows that the herbaceous habit and alternate leaves are the ancestral states in the tribe. The presence of stinging hairs is the derived status in Urticeae, and it might have been a key innovation triggering species diversification in the tribe.

Full text

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Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
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
;  || 
INTRODUCTION
 
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    
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Lam.
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
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

 
Poikilospermum 
                
        

Poikilospermum
            
   



   
 



   
Gyrotaenia
       
Generic phylogeny and character evolution in Urticeae (Urticaceae)
inferred from nuclear and plastid DNA regions
Changkyun Kim,1* Tao D e ng,1,2,3* Mark Chase,4 Dai-Gui Zhang,5 Ze-Long Nie1 & Hang Sun1
 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences,

  
 
 
  

 


DOI
   
Abstract
        
   
rbcLtrnLF
 
GyrotaeniaLaportea
       . Laportea              

ZhengyiaLaportea Nanocnide Dendrocnide Discocnide 
GirardiniaLaportea ObetiaPoikilospermum
 


Keywords

Supplementary Material



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 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record

Girardinia

 






     

       
rbcLtrnL      

Dendrocnide       
Discocnide  Laportea  
  


  
     
Laportea
ObetiaPoikilosper-
mum–
LaporteaL. cuspidata
––Zhengyia
   
Table 1.
 

Dendrocnide
.
Discocnide

Girardinia

Gyrotaenia



Laportea

      
      
      
      
      
      
 

    

 37     
 



mala



 






Nanocnide

Obetia

Poikilospermum


  L.
Zhengyia

   

  
      
      
    

 
      
      
 


 
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
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
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
  7 35  
  



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


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





67
Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
Version of Record
     


Nanocnide  Obetia
    


  
NanocnideGirardinia   
PoikilospermumDendrocnide
 




 
DendrocnideDiscocnideGirardiniaGyrotaeniaLaportea
NanocnideObetiaPoikilospermaZhengyia
 Zhengyia Nanocnide
 
  








rbcLtrnLF
    
      

     

MATERIALS AND METHODS
Taxon sampling. —
 



            
DendrocnideDiscocnideGirardinia
GyrotaeniaLaporteaNanocnideObetiaPoi-
kilospermum
      
Zhengyia
   
     

        
trnLF  
   Fatoua villosa 
Morus albaSorocea affinis 
    
Cannabis sabiva
lupulus   
rbcLtrnL-F

DNA isolation, PCR amplification, and sequencing. —



        
rbcL  
     
    
 rbcL  
 
   trnLF  

          
  

   




  
      

Phylogenetic analyses. —
   


     




trnL-F


   
 

 

     
     


     


   
  Laportea


     *     
   
    


TAX O N
 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record
Fig. 1.
 
A–E,

A,
Obetia radula 
B,
Poikilospermum
C,
Dendrocnide
amplissima 
D,
Zhengyia shennongensis
E,

F–G,
  
F,
Laportea cus-
pidata
G,
    
H,
Girardinia suborbiculatatriloba  
I–J,

I,
Zhengyia shen-
nongensis;
J,
Laportea bulbifera.
K–M,

K,
Poikilospermum
L,

  
M,

N,
Zhengyia shennongensis  
O–Q,

Dendrocnide basirotunda
P,
Laportea bulbifera
Q,
 

69
Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
Version of Record
    
   
 


       

  
    



     
      




Morphological character evolution. —


   


     


   
            
   


           






  


RESULT S
ITS and plastid analyses. —
 
    



          

 


 Gyrotaenia.
Gyrotaenia myriocarpa 


Laportea
. Laportea


rbcLtrnLF

 


Girardinia   
Discocnide–Dendrocnide– 
 Zhengyia–Laportea I–Nanocnide 
Gyrotaenia
Laportea
 
Laportea  
   
  Laportea
–Zhengyia–Laportea I–Nanocnide

 Laportea II




Table 2.


  rbcL trnLF 
     
  937   
     
     
  96  95 
     
     
     
     


TAX O N
 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record
Combined data analysis. —
  
          

    
Gyrotaenia myriocarpa

 Laportea
 
   
  Zhengyia–Laportea I–
Nanocnide  DendrocnideDiscocnide
Girardinia
 Laportea Obetia
Poikilospermum
Zhengyia shennongensis       
 
  Laportea  Nanocnide
Obetia
   
Poikilospermum


Morphological character evolution. —
   
   


          
   Dendrocnide
Discocnide  ObetiaPoikilospermum
       



              



Poik ilospermum

 


    
    

DISCUSSION
       





Phylogenetic position of Gyrotaenia. —
 
  Gyrotaenia 

Gyrotaenia

  

Gyrotaenia    
 

Gyrotaenia


                        

            Poi-
kilospermumGyrotaenia

Gyrotaenia
Elatostema
     Gyrotaenia
MyriocarpaPileaLecanthus  
ElatostemaGyrotaenia
     
 
Gyrotaenia 
Polyphyletic genera within Urticeae. —

DendrocnideDiscocnideGirardinia
NanocnideObetiaPoikilospermumZhengyia

Laportea

     
     




                   

  

    
     
 



  

Laportea  
    

         
      

Laportea
     


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Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
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Fig. 2.




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TAX O N
 –Kim & al. • Phylogeny and character evolution of Urticeae
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Fig. 3.

        
                    


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Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
Version of Record
-
pidata    

Laportea       

LaporteaSceptro-
cnide Fleurya      
Laportea
    
   

Laportea Sceptrocnide  


Laportea     
Laportea 
   -
sisFleurya
Laportea                   
   


  Laportea
Laportea
Laportea 



Laportea    
     
         
 –Zhengyia–Laportea I–Nanocnide
Laportea II–Obetia––
Poikilospermum         


   
 
   
      
   
Laportea   
       
  

ObetiaPoikilospermum   

Laportea          
  
     





     




    
  
 
   
 
   




 

 
    



    

  

 




Phylogenetic relationships within Urticeae. —



  
Zhengyia  Nanocnide–Laportea cus-
pidata   Zhengyia 
 
 
    

Zhengyia   

    
 Zhengyia  
     
   


Zhengyia

al
Nanocnide  
 


 

 Nanocnide   

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TAX O N
 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record

Laportea cuspidataLaportea
       Girardinia    
Laportea
   Girardinia    
   
 GirardiniaZhengyia   

 
  
  
Nanocnide
DendrocnideDiscocnide 

      
Dendrocnide


 Dendrocnide
   Dendrocnide 
Discocnide Dendrocnide

Discocnide
  
  

Girardinia diversifolia
    
     
Laportea
          
    
Girardina  Dendrocnide
Discocnide Laportea       
Girardina DendrocnideDiscocnide

  
   
diversifolia    
triloba     
     suborbidulata  

    

 diversifolia



       Laportea II
ObetiaPoikilospermum

Laportea   

    
    Obetia   
Poikilospermum–   III. 
ObetiaLaportea 
Girardinia
  Obetia 





Poikilospermum         
      
  
 


   
Poikilospermum
 
 
        

Poikilospermum
Poikilospermum



Poikilospermum   

 
  

Urticeae —
Poikilospermum.
 DendrocnideDiscocnide Girardinia
LaporteaNanocnideObetiaPoikilospermum
 Zhengyia.
Gyrotaenia.
Morphological character evolution. —
   


Zhengyia 


     



    


    
     


 



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Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
Version of Record
Akaike, H.    

   
Akbay, P., Basaran, A.A., Undeger, U. & Basaran, N. 
 
dioica L. 
   
Bassett, I.J., Crompton, C.W. & Woodland, D.W. 

     
Berg, C.C.    

Böhle, U.-R., Hilger, H.H. & Martin, W.F. 
Echium
 
 
Bonsen, K.J. & Ter Welle, B.J.H.           

Boufford, D.E.  
            Flora of North Amer-
ica

Boufford, D.E. & Spongberg, S.A.             





Burger, W.     Flora
Costaricensis   
 
Chen, C.J.   Sphaerotylos 
Acta

Chen, C.J., Lin, Q., Friis, I., Wi lmot-Dear, C.M. & Monro, A.K.
      
Flora of China 

Chew, W.L. Laportea     
Singapore
Clarke, L.A., Rebelo, C.S., Goncalves, J., Boavida, M.G. & Jordan,
P. 

 
Collier, H.O.J. & Chesher, G.B.  
         
Chemotherapy
  
Conn, B.J. & Hadiah, J.T.   

     
Deng, T., Kim, C., Zhang, D.G., Zhang, J.W., Li, Z.M., Nie, Z.L. &
Sun, H.  Zhengyia shennongensis
     
    
  
    
    


Echium
Lobelia




 DendrocnideLaportea
Laportea
     
       


     
  

    
     
     

   Euphorbia  
   
        
   
 
       



         
          

    
     
Poikilospermum
Poikilospermum 



 Laportea
    
    

Laportea

ACKNOWLEDGEMENTS
      
      
Y.      
     
    


     
  


   
LITERATURE CITED

76
TAX O N
 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record
Felsenstein, J. 
Evolution
 
Friis, I.   Girardinia          

Friis, I.  Obetia       
   
Friis, I.   
     Evolution, systematics, and
.

Friis, I.   
 
   
and Caryophyllid families 
Geltman, D.V.            
  
Hadiah, J.T. & Conn, B.J. 
 Elatostema    
Blumea
Hadiah, J.T., Conn, B.J. & Quinn, C.J. 


Horn, J.W., Van Ee, B.W., Morawetz, J.J., Riina, R., Steinmann,
V.W., Berry, P.E. & Wurdack, K.J. 
Euphor-
bia 
   
Joly, S., Starr, J.R., Lewis, W.H. & Bruneau, A. 
 
Bot 
Kato, T., Ishida, K. & Sato, H.       

    
Kelchner, S.A.      
 

Knox, E.B., Downie, S.R . & Palmer, J.D. 
    Lobelias

Li, H.L. 

   
Maddison, W.P. & Maddison, D.R.             

Monro, A.K. 
    Pilea 

  
Monro, A.K. & Rodríguez, A.            

    
Niklas, K.J. 
Evolution
 
Posada, D. & Crandall, K.A.  
Bioinformatics
      
Qian, H.     
      

    
Rambaut, A. & Drummond, A.J. 
 
Ronquist, F. & Huelsenbeck , J.P.    
   Bioinformatics 
  
Soltis, D.E., Mort, M.E., Latv is, M., Mavrodiev, E.V., O’Meara,
B.C., Solt is, P.S., Burleigh, J.G. & De Casas, R.R. 
                        
 
 
Steinmann, V.W. 

Swofford, D.L. *
*

Sytsma, K.J., Morawetz, J., Pires, J.C., Nepokroeff, M., Conti, E.,
Zjhra, M., Hall, J.C. & Chase, M.W.  
                   rbcL
trnLFndhF
   
Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J.          
         

  
Takhtajan, A.L. 
   
   
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. &
Higgins, D.G.    


 
Tuberville, T.D., Dudley, P.G. & Pollard, A.J.   

Laportea canadensis. Oikos 
 
Wang, W.T. & Chen, C.J.   
 
Weddell, H.A .     
Prodromus systematis naturalis regni vegetabilis

 
White, T.J., Birns, T., Lee, S. & Taylor, J. 

  
   -
tions
    
Woodland, D.W.  
Evolution,


Woodland, D.W., Bassett, I. J. & Crompton, C.W. 
            

Wu, Z.Y., Monro, A.K., Milne, R.I., Wang, H., Yi, T.S., Liu, J. & Li,
D.Z. 
 

      
Zhang, S.D., Soltis, D.E., Yang, Y., Li, D.Z. & Yi, T.S. 
     

     
Zurawski, G. & Clegg, M.T. 


 

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Kim & al. • Phylogeny and character evolution of Urticeae
TAX O N
 –
Version of Record
Appendix 1.
  
TRIBESpecies,  voucher specimen             rbcL  

URTICEAE Dendrocnide basirotunda     Deng 408**  *;
Dendrocnide basirotunda         Dendrocnide meyeniana 
      Dendrocnide urentissima
   ** *; Discocnide mexicana 
Girardinia diversifolia        diversifolia              
  Girardinia diversifoliadiversifolia      Girardinia
diversifolia diversifolia       Girardinia diversifolia diversifolia   
 Girardinia diversifolia suborbiculata
       Girardinia diversifolia triloba  
                 Girardinia diversifolia triloba
            Gyrotaenia myriocarpa   
       Hesperocnide sandwicensis       
    Hesperocnide sandwicensis           Hesperocnide
sandwicensis       Hesperocnide tenella
*  * *; Laportea alatipes       
   Laportea alatipes    
Laportea aestuans                      Laportea aestuans
       Laportea bulbifera 
* **; Laportea bulbifera   
   Laportea canadensis         
Laportea cuspidata** *; Laportea cuspidata
      Laportea interrupta
    Laportea interrupta           
 Laportea lanceolata                      
Laportea ruderalis  Laportea
ruderalisNanocnide japonica
    Nanocnide japonica  
Nanocnide lobata          Nanocnide lobata
Obetia aldabrensis  
Obetia pinnatifida       Obetia
radula       Obetia radula 
  Poikilospermum suaveolens                               
Poikilospermum suaveolens        **  *; Poikilospermum
sp. Poikilospermum sp. 
Poikilospermum sp. Urera baccifera
   Urera baccifera       
 Urera caracasana   Urera e lata
           Urera elata
   Urera fischeri         
Urera fischeri       Urera hypselodendron   
       Urera hypselodendron    
Urera hypselodendron 
Urera sansibarica  Urera sansibarica
Urera trinervis 
  Urtica dioica                 Urtica
dioica     Urtica fissa
            Urt ica f iss a            *
**; Urtica laetevirenslaetevirens  **  *;
Urtica laetevirens  dentata  * * *; Urtica
laetevirens  dentata          Urtica laetevirens  dentata 
          Urtica mairei         *
* *; Urtica maire i*  * *; Urtica mairei 
         Urtica massaica           
Urtica massaica       Urtica massaica  
         Urtica massaica    
    Urtica massaicaUrtica massaica
    Urtica massaica 
         Urtica massaica          
Urtica massaicaUrtica taiwaniana 
    Urtica taiwaniana Urtica
thunbergiana    Urtica thunbergiana
     Urtica triangularis             *
* *; Urtica triangularis * *   *; Urtica triangu-
laris     Zhengyiia shennongensis  
     *   **; Zhengyiia shennongensis             
  **  *BOEHMERIEAEBoehmeria clidemioides    
 Boehmeria penduliflora                 Boehmeria
sp.   EL ATOSTE MATEAE Elatostema ficoides  
         Elatostema stewardii     

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 –Kim & al. • Phylogeny and character evolution of Urticeae
Version of Record
  Pilea cavaleriei                      
Pilea plataniflora     * *    *; Pilea sinofasciata   
     Pilea sp.   
  FORSSKAOLEAEDroguetia iners                                
   Forsskaolea candida           PARIETAR-
IEAERousselia humilis                  Rousselia humilis
           OUTGROUPS: MORACEA EFatoua villosa  
    Morus alba   * * *; Sorocea affinis   *
  * *; Trophis racemosa  * * *CANNABACEAECannabis sativa     
       Humulus lupulus            
 
Appendix 1.



a      
Urticeae
Dendrocnide basirotunda 3
Dendrocnide meyeniana 3
Dendrocnide urentissima 3
 3
Girardinia diversifolia  diversifolia 
Girardinia diversifolia  suborbiculata 
Girardinia diversifolia  triloba 
 
 
Laportea aestuans 3
Laportea cuspidata 3
Laportea interrupta 3
Laportea ruderalis 3
 3
Nanocnide lobata 3
Obetia aldabrensis 3
Obetia pinnatifida 3
Obetia radula 3
Poikilospermum _ 
Poikilospermum _ 
Poikilospermum suaveolens 
 3
 3
 3
 3
 3
 3
 3
 3
 3
Appendix 2.
a, habit,
b, leaf arrangement,c, number of stipules, 
d, stipule position,e, achene shape, f, bulbils,
g, stinging hairs,h, number of tepals, 

Urticeae 
 dentata 3
 laetevirens 3
 3
 3
 3
 3
 3
Zhengyia shennongensis 3
Elatostemateae
Gyrotaenia myriocarpa 
Elatostema ficoides        
        
Pilea cavaleriei 
Pilea plataniflora 
Pilea sinofasciata 
Pilea         
Boehmerieae
Boehmeria clidemioides 
Boehmeria penduliflora 
Boehmeria        
Parietarieae
        
Forsskaoleae
Droguetia iners 
Forsskaolea candida 
Outgroups
Morus alba 
Fatoua villosa 
Cannabis sativa 
 


a      