Microscopic structures of Male & female reproductive organs LG1.
The Evolution of the Reproductive Organs of Maples, de ...
Transcript of The Evolution of the Reproductive Organs of Maples, de ...
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Analyses of morphology and flowering in light of the phylogeny
of the genus
The Evolution of the Reproductive Organs of Maples
Dr. Piet C. de Jong
(Von Gimborn Arboretum, Doorn, The Netherlands)
These slides were originally originally prepared in 2014, for a lecture to be given at the International Maple Symposium at the Morris Arboretum. This 2020 edition was prepared for the Maple Society Open Science Initiative by Emery Davis but contains only minor changes so that the slides will stand alone more clearly. A limited glossary was also added at the end in order to address a wider public.. All slides are copyright 2020 Piet C. de Jong and the Maple Society. Unauthorized distribution is prohibited.
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Female flowers in Acer
• Male sterility
• Competition with developing carpels cause anthers to
remain closed and filaments to not elongate
Acer platanoides
Acer rubrum
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Carpel abortion of male flowers before the female phase
• Cause: Competition for nutrients from the developing inflorescences (original mode)
Aesculus parviflora
Left : 2 month before floweringreduced inflorescence
Right: inflorescence near the endof flowering
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Carpel abortion of male flowers before the female phase
• Detached branches of protandrous flowering trees of a number of species were indoor forced into flower, starting in december.
• They all flowered protogynous (female→male).
• Forcing in later month showed on various moments a change to protandry (male→female).
• This change occured very late in Acer davidii subsp. grosseri and Acer maximowiczianum.
Experimental Investigation
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Aesculus parviflora(more and earlier appearing bisexual flowers )
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The effect of early removal of buds of female flowers in protogynous flowering trees of Acer
pseudoplatanus
• Removal shortly after leaf break resulted in a larger number of female flowers than in the entire inflorescense
• This effect decreased after removal on following days
• Example Acer pseudoplatanus ‘Corstorphinense’
• Between 20 April and 5 May in 1971 largest buds removed from 8-17 inflorescences
• Treatment 20-24 April resulted in 12.2-14.6 female flowers
• Treatment 25-27 April resulted in 2.6-9.1 female flowers
• Treatment 28 April to 5 May resulted in 0.3-1.1 female flowers
• No treatment resulted in 8.8 female flowers
(abstract of Table 22 in Flowering and Sex Expression in Acer L.)
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Heterodichogamy
• Protandry: male→ female
• Difference with the original duodichogamous mode of flowering is the early abortion of the carpels
• Protogyny: female→ male
• By contrast there is no carpel abortion in the oldest flower buds
Acer platanoides
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Heterodichogamy
• Most frequent mode of flowering in Acer
• Besides protandry (male→female) often duodichogamy (male→female→male) especially in case of large inflorescences
• Section Acer series Acer and Saccharodendron
• Section Ginnala
• Section Palmata
• Section Pentaphylla
• Section Platanoidea
• Section Pubescentia
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Duodichogamy
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♂-♀-♂
(de Jong 1976)
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2
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Acer pseudoplatanus (♂ Phase I)
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Acer pseudoplatanus (♂ Phase II)
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Androdioecy
• Part of the population is protogynous: female→male
• Remaining plants have male flowers and rarely female flowers (protandry)
• Carpel abortion very early after flower induction leading to very small rudimentary carpels
• Relatively small number of flowers
Section Glabra
Section Acer series Monspessulana
Section Hyptiocarpa
Section Rubra (p.p.) Acer saccharinumAcer sempervirens
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Dioecy
• Female flowers with or without rudimentary stamens
• Male flowers with very small rudimentary carpels
Section Arguta
Section Cissifolia
Section Indivisa
Section Lithocarpa (occasionaly
some protandrous inflorescences)
Section Negundo
Section Rubra (p.p.) Acer rubrumFemale flower, Section Lithocarpa
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Acer griseum
• Labile sex
• Inflorescences mainly male or female
• Trees genetically are protandrous or protogynous
Acer griseum
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Pollination
1. Entomophily: Insect pollination, original mode
2. Ambophily: both insect- and wind- pollination; drooping inflorescenses and flowers; flowers with protruding anthers and large stigmas.
3. Anemophily: Wind pollination, as well as the ambophilous characteristics, loss of discs and loss of anthers in female flowers; complete dioecy
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AnemophilyWind pollination
• Drooping inflorescences
• Large stigmas
• Loss of disc and petals
• Section Negundo, series Negundo
Acer negundo, male inflorescense Acer negundo, female inflorescense
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Evolution of inflorescences
• Reduction of size
• Shift to axillary buds and leafless shoots
• Loss of scorpioid structure
• Reduction to racemes and umbels
• Shift from erect to drooping
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Inflorescences of Acer
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Evolution of flowers1. Vanishing difference between sepals and petals
2. Intrastaminal disc >> amphistaminal disc >> extrastaminal disc >> complete disc reduction
3. 8 stamens >>> 5 stamens
4. Loss of stamens in female flowers
5. 5-merous flower >>> 4-merous flower with 4 stamens
6. Erect flower >> pendulous flower with long stalks (shift to wind pollination)
7. Drop of stamens of faded flowers >> complete flower drop
8. Partly drop of flower stalks of faded male flowers >> complete flower drop (loss of scorpioid cymes)
9. Increasing parthenocarpic tendency
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Acer cissifolium flowers 4-merous
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Evolutionary changes in fruit characteristics
1. Increasing parthenocarpic tendency
2. Thicker woody pericarp
3. Delayed seed germination
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Low parthenocarpic tendency
Acer saccharinum Acer nipponicum
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Moderate parthenocarpic tendency
Acer pseudoplatanus Acer davidii Acer japonicum
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Strong parthenocarpic tendency
Acer negundo Section Trifoliata (Acer mandshuricum)
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Evolutionary changes in number of bud scales
1. Original: no bud scales (Dipteronia)
2. Two pairs (Section Macrantha)
3. Two-three pairs (Acer spicatum)
4. Four pairs (Section Palmata)
5. Five-eight pairs (Section Platanoidea)
6. Eleven–fifteen pairs (Section Trifoliata)
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Bud scales, examples
Acer pensylvanicum (two pairs, connated) Acer palmatum (4 pairs, no terminal bud)
Acer pseudoplatanus (5-8 pairs)
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Evolutionary changes in leaf morphology
1. Original: Pinnated leaf (Acer negundo), Dipteronia
2. Palmate (5-lobed) (Acer pseudoplatanus, A. platanoides)
3. Pinnatilobed (Acer tataricum)
4. Trilobate (Acer monspessulanum)
5. Trifloliate leaf (Section Trifoliata, Section Cissifolia)
6. Digitate leaf (Acer pentaphyllum)
7. 7-11 Palmatilobed (Acer shirasawanum)
8. Entire (Acer carpinifolium, Acer laevigatum)
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Phylogeny of Acer (de Jong 1993)
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Subsequent molecular investigations to consider after de Jong’s phylogeny: Searching for
consensus
● Hasebe et al., Intrageneric relationships of maple trees based on chloroplast DNA Restriction Fragment Length Polymorphisms, 1998
● Suh et al., Phylogenetic relationships of maples, 2000
● Tian et al., Phylogeny of Aceraceae based on ITS and trn L-F data sets, 2000
● Li et al., Phylogenetics of Acer (Aceroideae, Sapindaceae) based on nucleotide sequences of two chloroplast non-coding regions, 2008
● And others
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Hasabe et al. 1998: Chloroplast DNA RFLPs Phylogeny of Acer
Remarks:
● Acer caesium and A. heldreichii monophyletic
● Acer pseudoplatanus in same cluster but Section Acer not monophyletic: Series Monspessulana apart
● Acer distylum and A. nipponicum monophyletic
● Acer spicatum and A. caudatum subsp. ukurunduense [Acer ukurunduense (Trautvetter & Meyer) Murray (1966)] monophyletic
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Suh et al. Phylogenetic relationships (2000):
Remarks:
● Small number of species
● Acer distylum and A. nipponicum monophyletic
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Tian et al., 2000
Remarks:
• Acer distylum and A. nipponicum monophyletic
• Acer caesium and A. heldreichii subsp. trautvetteri monophyletic
• Section Acer not monophyletic, but A. opalus and A. saccharum monophyletic
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Li et al. (2006)
Remarks:
• Acer distylum and A. nipponicum in different clades
• Species of Series Acer in 3 different clades
• Acer pseudoplatanus and A. glabrum monophyletic
• Acer spicatum and A. caudatum subsp. ukurunduense in different clades
• Acer spicatum and A. carpinifolium monophyletic
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Consensus with monophyletic sections and series
• Section Acer series Monspessulana
• Series Arguta
• Section Ginnala
• Section Integrifolia
• Section Lithocarpa
• Section Macrantha
• Section Palmata
• Section Platanoidea
• Section Rubra (related to Section Hyptiocarpa)
• Section Trifoliata
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Different or doubtful results?
• Acer caesium and A. pseudoplatanus not related to remaining species of Series Acer
• Acer glabrum monophyletic with A. pseudoplatanus
• Acer caesium monophyletic with A. pilosum
• Acer spicatum more closely related to A. carpinifolium than to A.
caudatum
• Acer distylum of sect. Parviflora is more closely related to Section Platanoidea than to A. nipponicum of Section Parviflora
• Acer caudatum and A. spicatum not related to A. distylum and A. nipponicum
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Acer glabrum versus A. pseudoplatanusFlower morphology does not support monophyly
A. glabrum
A. pseudoplatanus
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Acer caesium versus Acer pilosumMorphology does not support monophyly
Acer caesiumAcer pilosum
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Acer caudatum versus A. spicatumFlower morphology suggests very close relationship or monophyly
Acer caudatum
Acer spicatum
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Phylogeny HippocastanoideaeBUERKI ET AL.(2010)
A second possible alternative?
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Consider Dipteronia:
Results differ between Buerki, Tian, Yang.
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Tian et al. (2002)
Remarks:
• Dipteronia not monophylectic
• D. dyerana in clade with Section Parviflora
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Distribution of Dipteronia
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What is the phylogenetic placement of Dipteronia dyerana? Yang et al. (2010)
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Jianhua Li, Jipei Yue, Suzanne Shoup (2006)
The Authors Conclude:
More data are needed to fully resolve the
intersectional relationships of Acer.
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Afterword from the Editor, May 2020
Maple phylogeny and biogeography inferred from phylogenomic data, Li et al, 2019
The Authors Conclude:
“… the first study that has resolved the basal relationships of Acer using DNA sequence data from over 500 nuclear loci generated via the anchored hybrid enrichment method.
All of the sections sensu de Jong (2004) [2002 ed.] are supported except for section Pentaphylla, which is paraphyletic containing section Trifoliata, while few of the sectional groups as proposed by other previous researchers are monophyletic. ...”
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Selected Online Resources• Flowering and Sex Expression in Acer L., P.C. de Jong, 1976 http://edepot.wur.nl/206182
• Phylogeny and circumsciption of Sapindaceae revisited, Buerki et al, 2010.
http://www.missouribotanicalgarden.org/Portals/0/staff/PDFs/callmander/Buerkietal.2010.pdf
• Phylogeny of Aceraceae based on ITS and trnL-F data sets, Tian et al, 2000
https://www.researchgate.net/publication/236590342_Phylogeny_of_Aceraceae_based_on_ITS_and_trnL-F_data_s
ets
• Phylgenetics of Acer (Aceroideae, Sapindaceae)… Li et al, 2008
http://flora.huh.harvard.edu/china/harvard_papers/li_yue_shoup_101_115.pdf
• Worldwide Maple Diversity, de Jong, 2002
https://maplesociety.org/sites/default/files/deJongWorldwideMapleDiversity-vf.pdf
• Intrageneric relationships of maple trees, Hasebe et al, 1998 https://link.springer.com/article/10.1007/BF02507809
• Phylogenetic Relationships of Maples, Suh et al, 1998.
https://www.researchgate.net/publication/225166562_Phylogenetic_Relationships_of_Maples_AcerL_Aceraceae_
Implied_by_Nuclear_Ribosomal_ITS_Sequences
• The Evolution of Dioecy, Heterodichogamy, and Labile Sex Expression in Acer, Renner et al, 2007
https://www.umsl.edu/~renners/Acer_Evolution2007.pdf
• Phylogeny and Correlated Evolution in Maples, Ackerly et al, 1998
https://donoghuelab.yale.edu/sites/default/files/079_ackerly_amnat98_0.pdf
• A Nuclear Ribosomal DNA Phylogeny of Acer, Grimm et al, 2006
http://www.umsl.edu/~renners/Grimm_etal_Acer_2006.pdf
• What is the phylogenetic placement of Dipteronia dyerana Henry?
https://www.tandfonline.com/doi/abs/10.1080/11263504.2010.490032?mobileUi=0&journalCode=tplb20
• Maple phylogeny and biogeography inferred from phylogenomic data, Li et al, 2019
https://onlinelibrary.wiley.com/doi/epdf/10.1111/jse.12535
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Selected GlossaryAmbophily – Both insect and wind pollination.
Andromonoecy – Both bisexual and male flowers on the same plant.
Anemophily – Wind pollination.
Dioecy – Having either male or female flowers on a single plant.
Duodichogamy – Characterized by flowering in the sequence male, female, male.
Entomophily – Insect pollination
Heterodichogamy – Presence of male and female characteristics, at different times, in a flower.
Merosity – Number of parts, e.g. 4-merous, having 4 petals.
Monoecious – Having both male and female flowers on the same plant.
Monophyletic – Descendants of a common ancestor with shared derived characteristics.
Pericarp – Outermost layer, or husk or a ripe fruit.
Protandry – Male flower parts maturing before female parts.
Parthenocarpy – Production of seedless fruit, without fertilization.
Phylogenetics – The study of evolutionary relatedness through molecular sequencing and morphological data.
Protogyny – Female flower parts maturing before male parts.