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Reconceptualizing
morphology:
The architecture of a
giant single-celled alga
& the latent shapes of
grapevine leaves
Dan Chitwood
Donald Danforth Plant Science Center
September 28, 2015
A giant single-celled alga
& the implications for plant
cell theory
Latent genetic &
developmental shapes in
grapevine leaves
The shape of climate change:
Inter-annual variability in
grapevine leaf shape
Independent origins of multicellularity
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
M Abedin & N King (2010)
Trends in Cell Biology
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
M Abedin & N King (2010)
Trends in Cell Biology
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
M Abedin & N King (2010)
Trends in Cell Biology
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
Independent origins of multicellularity
Opisthokonts
Streptophytes
Viridiplantae
Plantae
Chlorophytes
Rhodophytes
Algae
(polyphyletic)
Macroscopic morphological complexity:
plant architecture without multicellularity
V Coneva & D Chitwood (2015)
Front Plant Sci
Adapted from Cocquyt et al.
(2010) Mol Biol Evol
Macroscopic morphological complexity:
plant architecture without multicellularity
Hämmerling, 1930s
www.science-projects.com
Macroscopic morphological complexity:
plant architecture without multicellularity
V Coneva & D Chitwood (2015)
Front Plant Sci
Adapted from Cocquyt et al.
(2010) Mol Biol Evol
Macroscopic morphological complexity:
plant architecture without multicellularity
Ernst Haeckel, Wikipedia,
Wikimedia commons
Cell vs. Organismal Theory:
Plant development ≠ Animal development
Kaplan and Hagemann (1991)
BioScience
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
Kaplan and Hagemann (1991)
BioScience
Cilia and Jackson (2004)
Curr Opin in Cell Biol
Kaplan and Hagemann (1991)
BioScience
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
2) Phragmoplasts
Kaplan and Hagemann (1991)
BioScience
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
2) Phragmoplasts
3) Cell lineage patterns
Kaplan and Hagemann (1991)
BioScience
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
2) Phragmoplasts
3) Cell lineage patterns
Brukhin, Curtis, Grossniklaus (2005)
Current Science
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
2) Phragmoplasts
3) Cell lineage patterns
4) Coenocytic female gametophyte
Kaplan and Hagemann (1991)
BioScience
Cell vs. Organismal Theory:
Plant development ≠ Animal development
1) Plasmodesmata, symplasm
2) Phragmoplasts
3) Cell lineage patterns
4) Coenocytic female gametophyte
Conclusion: there is as much evidence to view
morphologically complex plants as coenocytes as
there is to consider them multicellular (at least in the
same sense as animals)
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Why Caulerpa taxifolia?
1) Debatably world’s largest single-
celled organism
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Why Caulerpa taxifolia?
1) Debatably world’s largest single-
celled organism
2) Can regenerate from any fragment
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Why Caulerpa taxifolia?
1) Debatably world’s largest single-
celled organism
2) Can regenerate from any fragment
3) “Killer algae”—invasive
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Why Caulerpa taxifolia?
1) Debatably world’s largest single-
celled organism
2) Can regenerate from any fragment
3) “Killer algae”—invasive
4) Endosymbiotic bacteria
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Why Caulerpa taxifolia?
1) Debatably world’s largest single-
celled organism
2) Can regenerate from any fragment
3) “Killer algae”—invasive
4) Endosymbiotic bacteria
5) Convergent morphology with land
plants
Ranjan et al. (2015)
PLOS Genetics
An intracellular transcriptomic atlas of the
giant coenocyte Caulerpa taxifolia
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
A “wave” of apical-basal
gene expression
Ranjan et al. (2015)
PLOS Genetics
Intracellular patterns
of gene expression
coincide with pseudo-
organs
Ranjan et al. (2015)
PLOS Genetics
Intracellular patterns
of gene expression
coincide with pseudo-
organs
Ranjan et al. (2015)
PLOS Genetics
Molecular homology between land plant
organs and algal pseudo-organs?
Leliaert et al.
(2012)
Crit. Rev.
Plant Sci.
Molecular homology between land plant
organs and algal pseudo-organs?
Ranjan et al. (2015)
PLOS Genetics
Molecular homology between land plant
organs and algal pseudo-organs?
Ranjan et al. (2015)
PLOS Genetics
??
D Reinhardt
Molecular homology between land plant
organs and algal pseudo-organs?
Ranjan et al. (2015)
PLOS Genetics
?
Molecular homology between land plant
organs and algal pseudo-organs?
Ranjan et al. (2015)
PLOS Genetics
Molecular homology between land plant
organs and algal pseudo-organs?
Ranjan et al. (2015)
PLOS Genetics
D Reinhardt
A giant single-celled alga
& the implications for plant
cell theory
Latent genetic &
developmental shapes in
grapevine leaves
The shape of climate change:
Inter-annual variability in
grapevine leaf shape
Species effects
Species, developmental stage,
& leaf number effects
Species, developmental stage,
& leaf number effects
Species, developmental stage,
& leaf number effects
Shoot
base
Shoot
tip
Species, developmental stage,
& leaf number effects
L1 L2
L1
L3 L4 L5 L6 L7 L8 L9 L10
Shoot
base
Shoot
tip
Leaf
Number,
different leaf types
Species, developmental stage,
& leaf number effects
S1S2S9S10 S3S4S5S6S7S8
L1 L2
L1
L3 L4 L5 L6 L7 L8 L9 L10
Developmental
Stage,
unequal expansion
Leaf
Number,
different leaf types
Shoot
base
Shoot
tip
Species, developmental stage,
& leaf number effects
Shoot
base
Shoot
tip
Leaf number
Developmental stage
Unequal expansion
Different leaf types
Species, developmental stage,
& leaf number effects
Shoot
base
Shoot
tip
Leaf number
Developmental stage
Unequal expansion
Different leaf types
Species, developmental stage,
& leaf number effects
Shoot
base
Shoot
tip
Leaf number
Developmental stage
Unequal expansion
Different leaf types
Evolutionary vs. developmental paths
in the Vitis leaf morphospace
Species effects
Evolutionary vs. developmental paths
in the Vitis leaf morphospace
Developmental stage
Unequal expansion
Evolutionary vs. developmental paths
in the Vitis leaf morphospace
Leaf number
Different leaf types
Species identity can be predicted
independently from development
Species identity can be predicted
independently from development
Developmental stage can be predicted
independently from species identity
Leaf number can be predicted
independently from species identity
A giant single-celled alga
& the implications for plant
cell theory
Latent genetic &
developmental shapes in
grapevine leaves
The shape of climate change:
Inter-annual variability in
grapevine leaf shape
Landmarks sensitive to allometry
Blade expands faster than vein
Blade expands faster than vein
Blade expands faster than vein
Genetic & developmental shapes are independent
Genetic & developmental shapes are independent
Genetic & developmental shapes are independent
Genetic & developmental shapes are independent
Discriminating leaves from different years:
Same vines, same stages
Discriminating leaves from different years:
Same vines, same stages
Discriminating leaves from different years:
Same vines, same stages
Discriminating leaves from different years:
Same vines, same stages
Climate interannual variability:
2014/15 was colder & drier than 2012/13
Climate interannual variability:
2014/15 was colder & drier than 2012/13
Extant and geologic history:
Leaf shape & size correlate with climate
Extant and geologic history:
Leaf shape & size correlate with climate
Paleomap, scotese.com
Thanks!
Caulerpa
Aashish Ranjan
Brad Townsley
Yasu Ichihashi
Neelima Sinha
Grapes
Laura Klein
Allison Miller
Jason Londo
Susan Rundell
Quaneisha Woodford
Darren Li
Tommy Yu
Jose Lopez
Julie Kang
Tomatoes/grafting
Margaret Frank
Viktoriya Coneva
The morphospace of
wild & domesticated Vitis
The morphospace of
wild & domesticated Vitis
Changes in developmental timing
in domesticated grape

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Reconceptualizing morphology: The architecture of a giant single-celled alga & the latent shapes of grapevine leaves