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The Impact of Recent DNA The Impact of Recent DNA Studies on the Classification Studies on the Classification
of Section Pæonia of Section Pæonia
Presentation to the International Peony Symposium
Munich, Germany
7 May 05
Don SmithDon SmithWest Newton, Massachusetts
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Summary of Modern Summary of Modern DNA Sequence StudiesDNA Sequence Studies
Analysis of DNA sequences is an extremely Analysis of DNA sequences is an extremely powerful tool for reconstructing complex powerful tool for reconstructing complex evolution patterns in plantsevolution patterns in plants
Recent studies applied to Peonies have uncovered some surprising new results
•The majority of species in section Pæonia are of hybrid origin •P. tenuifolia, p. anomala, p. veitchi and p. lactiflora are probably the only species in section pæonia not derived from natural hybridization
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Tao SangTao Sang Associate ProfessorPh.D., Ohio State U.
Department of Plant BiologyMichigan State UniversityEast Lansing, MI 48824-1312 USAPhone: (517) 355-4689Fax: (517) 353-1926e-mail:[email protected]
Plant Biology DepartmentEcology, Evolutionary Biology & Behavior ProgramGenetics Graduate ProgramCollege of Natural Science
The Peony GuruThe Peony Guru
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Recent DNA Studies Recent DNA Studies on Genus Pæoniaon Genus Pæonia
1. 1. Sang, T., Crawford, D. J., & Stuessy, T.F. (1995) Sang, T., Crawford, D. J., & Stuessy, T.F. (1995) Proc. Natl. Acad. Sci USAProc. Natl. Acad. Sci USA 92, 6813-6817.92, 6813-6817.
2.2. Sang, T., Crawford, D. J., & Stuessy, T.F. (1997) Sang, T., Crawford, D. J., & Stuessy, T.F. (1997) Am. J. Bot.Am. J. Bot. 84, 1120-1136. 84, 1120-1136.
3.3. Sang, T. & Zhang, D. (1999) Sang, T. & Zhang, D. (1999) Syst. Bot.Syst. Bot. 24, 148-163. 24, 148-163.
4.4. Sang, T., Donoghue, M.J. & Zhang, D. (1997) Sang, T., Donoghue, M.J. & Zhang, D. (1997) Mol. Biol. Evol.Mol. Biol. Evol. 14, 994-1007. 14, 994-1007.
5.5. Ferguson, D. & Sang, T., (2001) Ferguson, D. & Sang, T., (2001) Proc. Natl. Acad. Sci USAProc. Natl. Acad. Sci USA 98, 3915-3919. 98, 3915-3919.
6.6. Sang, T. (1995) Doctoral Dissertation, Ohio State University.Sang, T. (1995) Doctoral Dissertation, Ohio State University.
7.7. Zhang, D. & Sang, T. (1999) Zhang, D. & Sang, T. (1999) Am. J. Bot.Am. J. Bot. 86 (5), 735-740. 86 (5), 735-740.
8.8. Zhang, D. & Sang, T. (1998) Zhang, D. & Sang, T. (1998) Genome.Genome. 41 (6), 848-853. 41 (6), 848-853.
9.9. Tank, D.C. & Sang, T. (2001) Tank, D.C. & Sang, T. (2001) Mol. Phylogenet Evol.Mol. Phylogenet Evol. 19 (3), 421-429. 19 (3), 421-429.
10.10.Sang, T. (2002) Sang, T. (2002) Critical Reviews in Biochemistry and Molecular BiologyCritical Reviews in Biochemistry and Molecular Biology 37: 37: 121-147.121-147.
11.11.Sang, T. and Y. Zhong. (2000) Sang, T. and Y. Zhong. (2000) Systematic BiologySystematic Biology 49: 422-434. 49: 422-434.
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Major Conclusions of Major Conclusions of Recent DNA Studies on Recent DNA Studies on
Genus PæoniaGenus Pæonia
Various recent DNA sequence studies support Various recent DNA sequence studies support the grouping of the genus into three (3) the grouping of the genus into three (3) sections as proposed by Stern in 1946. These sections as proposed by Stern in 1946. These sections are:sections are:
MoutanMoutan
OnæpiaOnæpia
PæoniaPæonia
Classification of the largest section (Pæonia) is complicated by the finding that significant natural hybridization has occurred within the section.
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Species Tree for Genus Pæonia
|----- Section Moutan ---- | Section Onæpia |----------------------------------- Section Pæonia --------------------------------|
Vaginatae Delavayanae P. californica P. lactiflora P. veitchii P. tenuifolia P. anomalaSubsection Subsection P. brownii
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Key DNA Study on Key DNA Study on Genus PæoniaGenus Pæonia
• The results and conclusions presented in this talk The results and conclusions presented in this talk are based on numerous recent studies by Sang et are based on numerous recent studies by Sang et al. The most important of these landmark studies al. The most important of these landmark studies is listed below:is listed below:
– Sang T., Crawford J. D., Stuessy T. F., Chloroplast DNA phylogeny, reticulate evolution and biogeography of Pæonia (Pæoniaceae), American Journal of Botany, 84 (8), 1120-1136, 1997.
• The phylogeny charts which follow are based primarily on Figure 7 (page 1131) from the above paper, but have been modified to include the results of more recent studies.
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Phylogeny of Section Pæonia
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
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Time (~ 10 million years)
Phylogeny of Section Pæonia
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-J AP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
Decreasing degree of foliage dissection
Increasing degree of foliage dissection
= Hybrid species ESx = Extinct species= Male Parent = Female Parent= Parent of unknown gender
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Time (~ 10 million years)
Ancient Time Present Day
Phylogeny of Section Pæonia
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-J AP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
Decreasing degree of foliage dissection
Increasing degree of foliage dissection
Approx. Time (~ 10 Million Years)
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Non-hybrid species inNon-hybrid species in goldgold
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Descendents of Ancient Species 1 (AS1) in Red
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
AS1
AS2
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Pure Descendents of Ancient Species 1 (AS1) in Orange
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
AS1
AS2
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Descendents of Ancient Species 2 (AS2) in Green
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
AS1
AS2
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Pure Descendents of Ancient Species 1 (AS1) in Orange
Descendents of Ancient Species 2 (AS2) in green
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
AS1
AS2
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Phylogeny of Section PæoniaPhylogeny of Section Pæonia Stern’s Section Dissectifoliae
Stern’s Section Foliolatae
ES1
ES2
ES3
TEN
ANO
PER
VEI
OFF
ARI-PAR
XIN
EMO
OBO-JAP
WIT
BAN
STE
LAC
CLU-MAS
CAM-RUS
MAI
AS1
AS2
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DNA Sequence DNA Sequence AnalysisAnalysis
•Analyzing both nuclear and chloroplast (maternally Analyzing both nuclear and chloroplast (maternally inherited) DNA sequences allows identification of:inherited) DNA sequences allows identification of:
Hybrid species
Parental species (often including identification of maternal & paternal parents)
Groups of closely related species sharing the same parentage (“Sister Groups”)
Number and order of hybridization events (identification of double, triple, quad hybrids)
Approx. time of origin (i.e., when the new hybrid species was created)
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Surprising Surprising ConclusionsConclusions
Two of the more surprising conclusions of Two of the more surprising conclusions of these DNA sequence studies are:these DNA sequence studies are:
The high proportion of diploids among the hybrid species (9 of 21)
• Hybrid species in nature are most often polyploids
Most of the hybrid species are found in the Mediterranean region whereas their parental species are presently restricted to Asia
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Summary of the Summary of the Extinct Species in Extinct Species in Section PæoniaSection Pæonia
•DNA sequence studies have DNA sequence studies have established that established that threethree (3) ancient (3) ancient species in section Pæonia are extinct:species in section Pæonia are extinct:
Fortunately, many descendents of these extinct species still exist
This is known because the “fingerprints” (DNA sequences) of these ancient species can still be seen in the genes of their descendents.
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Hybrid Distribution Hybrid Distribution of Section Pæonia of Section Pæonia
SpeciesSpeciesHybrid Distribution of Hybrid Distribution of
Species in Species in SectionPæoniaSectionPæonia
Non-hybrids (4) = 16%
Single Hybrids (6) = 24%
Double Hybrids (10) = 40%
Triple/Quad Hybrids (5) = 20%
Total Hybrids (21) = 84%
Total Species = 25
N on-hyb
Sgle Hyb
Dble Hyb
Tri+ Hyb
Non-hybrid species make-up only about 1/6 of the total
N on-hyb
Sgle Hyb
Dble Hyb
Tri+ Hyb
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Hybrid Status of Hybrid Status of Species in Section Species in Section
PæoniaPæoniaSummary of the 25 Species in Section Summary of the 25 Species in Section
PæoniaPæonia
Non-Hybrid Species
Single Hybrid Species
Double Hybrid Species
Triple or Quad Hybrid Species
Anomala Mairei Peregrina Wittmanniana (4) Veitchii Emodi Sterniana Banatica
Tenuifolia Xinjiangensis Clusii Obovata Lactiflora Arietina Rhodia Japonica
Humilis Broteri Officinalis (4) Parnassica Coriacea Mlokosewitschi Mascula Cambessedesii Russi 4 6 10 5
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Hybrid Species Produced Hybrid Species Produced by Other Species in by Other Species in
Section PæoniaSection PæoniaNumber of times each species in Section Pæonia
was a parent of another hybrid species
Species No. of Hybrids
Species No. of Hybrids
Anomala 1 Xinjiangensis 0
Veitchii 2 Sterniana 0
Tenuifolia 1 Cambessedesii 0
Lactiflora 4 Russi 0
Mairei 3 Wittmanniana 0
Emodi 1 Banatica 0
Arietina - Parnassica 5 Obovata 0
Clusii - Mascula 1 Japonica 0
Peregrina 1 Officinalis 0
Extinct Species 1 1
Extinct Species 2 2
Extinct Species 3 1
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Distribution of Hybrid Distribution of Hybrid Species in Section Species in Section
PæoniaPæonia
Ancient Species Intermediate
Species
Modern
Species
Tenuifolia Emodi, Xinjiangenis
Sterniana
Anomala Cambessedesii, Russi
Banatica
Veitchi Peregrina Officinalis
Lactiflora Wittmanniana
Mairei
Clusii – Mascula Group
Obovata, Japonica
Arietina – Parnassica Group
Species grouped by relative age
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““Sister” Groups in Sister” Groups in Section PæoniaSection Pæonia
Ari – Par
Group
Clusii – Mascula
Group
Obovata –
Japonica Group
Arietina Clusii Obovata
Humilis Rhodi Japonica
Parnassica Broteria
Coriacea
Mlokosewitschi
Mascula
Species which share the same parents are grouped into “sister” groups
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““Sister” Groups in Sister” Groups in Section Pæonia Section Pæonia
(Cont’d)(Cont’d)
Cam – Rus Group Emo – Xin Group
Cambessedesii Emodi
Russi Xinjiangenis
Species which share the same parents are grouped into “sister” groups
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Closely Related Closely Related Species That Share a Species That Share a
Single ParentSingle Parent
Per – Off Group Ban – Ste Group
Peregrina Banatica
Officinalis Sterniana
Species which share one parent can be grouped into “step-sister” groups
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Distribution of Distribution of Descendents in Descendents in Section PæoniaSection Pæonia
Descendents of
AS1
Descendents of
AS2
Descendents of
Both
Tenuifolia Mairei Cambessedesii,
Russi
Anomala Extinct Species
2
Clusii – Mascula
Group
Veitchi Sterniana
Lactiflora Banatica
Emodi,
Xinjiangenis
Obovata, Japonica
Peregrina,
Officinalis
Wittmanniana
Ari – Par Group
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Impacts on the Impacts on the Classification Classification of the Genusof the Genus
Extensive natural hybridization within section Extensive natural hybridization within section pæonia has made the classification of this section pæonia has made the classification of this section extremely difficultextremely difficult
Attempts to classify the herbaceous peonies solely from morphological characteristics without the knowledge of which species were derived from hybridization, will undoubtedly lead to inaccurate and erroneous results
•Therefore, all previous peony classifications based solely on morphological characteristics must be viewed as inadequate and thus should be rejected
– This includes the recent classification presented in the new Halda book, The Genus Pæonia
•Since the majority of species in section Pæonia are of hybrid origin, identification of these hybrid species is essential to an accurate classification of this section
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Section Pæonia Section Pæonia Classification Classification RestrictionsRestrictions
•For the purposes of classification, For the purposes of classification, species in “sister” groups and “step-species in “sister” groups and “step-sister” groups must remain together :sister” groups must remain together :
This limits the classification problem to the grouping of only 13 distinctly separate groups
4 non-hybrid species + 9 hybrid species groups
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Classification Options Classification Options for Section Pæoniafor Section Pæonia
Sub-section 1 Sub-section 2 Sub-section 3
Tenuifolia Mairei (Cambessedesii,
Russi)
Anomala Clusii – Mascula
Group
Veitchi Sterniana
Lactiflora Banatica
(Emodi,
Xinjiangenis)
(Obovata,
Japonica)
(Peregrina,
Officinalis)
Wittmanniana
Ari – Par Group
Option 1
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Classification Options Classification Options for Section Pæoniafor Section Pæonia
Sub-section 1 Sub-section 2
Tenuifolia Mairei
Anomala (Cambessedesii,
Russi)
Veitchi Clusii – Mascula
Group
Lactiflora Sterniana
(Emodi,
Xinjiangenis)
Banatica
(Peregrina,
Officinalis)
(Obovata,
Japonica)
Ari – Par Group Wittmanniana
Option 2
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Comparison of Comparison of Classifications for Classifications for Section PæoniaSection Pæonia
Sub-section 1 Sub-section 2
Tenuifolia Only 4 of the 25
speciesMairei
Anomala were placed
differentlyCambessedesii,
Russi
Veitchi by Stern Clusii – Mascula
Group
Lactiflora Sterniana
Emodi,
Xinjiangenis
Banatica
Peregrina,
Officinalis
Obovata, Japonica
Ari – Par Group Wittmanniana
Comparison with Classification of Stern(1946)
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Classification Options Classification Options for Section Pæoniafor Section Pæonia
Sub-section 1(Dissectifolae)
Sub-section 2(Foliolatae)
Sub-section 3(Intermediatae)
Tenuifolia Lactiflora (Obovata,
Japonica)
Anomala Mairei Sterniana
Veitchi (Cambessedesii,
Russi)
Banatica
Ari – Par Group Clusii – Mascula
Group
Wittmanniana
(Peregrina,
Officinalis)
Extinct Species 1 (Emodi,
Xinjiangenis)
Extinct Species 3 Extinct Species 2
Option 3
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Proposed Re-Proposed Re-classification for classification for Section PæoniaSection Pæonia
Dissectifoliae Foliolatae
Tenuifolia Mairei
Anomala Cambessedesii,
Russi
Veitchi Clusii – Mascula
Group
Lactiflora Sterniana
Emodi,
Xinjiangenis
Banatica
Peregrina,
Officinalis
Obovata, Japonica
Ari – Par Group Wittmanniana
Proposed classification of Section Pæonia based on the work of Sang et al.
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Halda’s Proposed New Halda’s Proposed New Classification of Genus Classification of Genus
PæoniaPæonia
Albiflor
a
Emodi Paeonia Tenuifoli
ae
Flavonia
Lactiflora
Emodi Peregrina, Officinalis, Banatica
Tenuifolia
Mlokosewitschii
Sterniana Ari – Par Group Wittmanniana
Clusii – Mascula Group
Cambessedesii, Russi
Anomala, Veitchi, Xinjiangensis
Obovata, Japonica, Mairei
Classification of Genus Pæonia proposed by Halda
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Comments on Comments on Halda’s Halda’s
New ClassificationNew ClassificationHalda’s new classification of the genus does Halda’s new classification of the genus does not hold up in the light of these recent DNA not hold up in the light of these recent DNA sequence studies :sequence studies :
There is no DNA evidence to support the placing of p. lactiflora as a separate Sub-genus or even a separate Section. At best, p. lactiflora could only be treated as a separate sub-section under Section Paeonia
Likewise, there is no evidence to support a separate section (or even a sub-section) for Tenuifolia or Emodi
In addition, there is nothing to support placing the two yellow species, p. mloko and p. wittmanniana, into a separate section (or sub-section)
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Parentage of Hybrid Parentage of Hybrid Species in Section Species in Section
PæoniaPæonia
Maternal Parent Paternal Parent Hybrid Species (11)
Lactiflora x Veitchii = Xinjiangensis
Veitchii x Lactiflora = Emodi
Emodi x Mairei = Sterniana
Ancient Species 1 x Unknown extinct species 1 = Mairei
Arietina-Parnassica Group x Clusii-Mascula Group = Wittmanniana
Arietina-Parnassica Group x Mairei = Banatica
Arietina-Parnassica Group x Unknown extinct species 2 = Obovata
Arietina-Parnassica Group x Unknown extinct species 2 = Japonica
Unknown extinct species 3 x Tenuifolia = Arietina
Unknown extinct species 3 x Tenuifolia = Humilis
Unknown extinct species 3 x Tenuifolia = Parnassica
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Parentage of Hybrid Parentage of Hybrid Species in Section Species in Section
PæoniaPæonia
Parent 1 Parent 2 Hybrid Species (10)
Anomala x Arietina- Parnassica Group = Peregrina
Lactiflora x Unknown extinct species 2 = Clusii,
Rhodia,
Broteri
Lactiflora x Unknown extinct species 2 = Coriacea,
Mloko,
Mascula
Lactiflora x Mairei = Cambessedesii, Russi
Arietina-Parnassica Group x Peregrina = Officinalis
Arietina- Parnassica Group = Arietina, Humilis, and Parnassica Clusii-Mascula Group = Clusii, Rhodia, Broteri, Coriacea, Mlokosewitschi, Mascula
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Conclusions of Recent Conclusions of Recent DNA Studies on DNA Studies on
PæoniaPæonia
Analysis of recent DNA data supports the Analysis of recent DNA data supports the classification of the genus into three (3) classification of the genus into three (3) sections :sections :
MoutanMoutan
OnæpiaOnæpiaPæoniaPæonia
Classification of the largest section (Pæonia) is complicated by the fact that significant natural hybridization has occurred within the section.
• However, it appears that only 2 or at most 3 sub-sections are needed to adequately group the approximately 25 species which make up this section
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On-line Copy of This On-line Copy of This PresentationPresentation
A copy of this presentation will be A copy of this presentation will be
posted on-line at my websiteposted on-line at my website www.paeonianewsletter.comwww.paeonianewsletter.com