2/26/2014
Petaloidy, Polarity and
Pollination:
Zingiberales : a model clade of monocots
The evolution and
diversification of floral form in
the Zingiberales
Chelsea D. Specht, Roxana Yockteng, Ana M.R. Almeida
University of California - Berkeley
Department of Plant and Microbial Biology, Integrative Biology &
The University and Jepson Herbaria
APGII 2003
Zingiberales phylogeny
Banana families
Ginger families
sensu Kress et al 2001
Zingiberales floral evolution
Banana families
Ginger families
sensu Kress et al 2001
Fitness & Evolution of Form?
Inferences of Homology:
Position? Transition? Structure? History?
Remane 1971
SEPALS
Almeida, Brown & Specht. 2013. AoB PLANTS
PETALS
STAMENS
STAMENS
CARPELS
Wake, Wake & Specht 2011 Science
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Trend 1: Reduction in fertile stamen number/ increase in ‘petaloidy’
SEPALS
PETALS
STAMENS
STAMENS
CARPELS
SEPALS
Wake, Wake & Specht 2011 Science
B
C
C
CARPELS
CARPELS
TEPALS
Sepals
TEPALS
labellum
STAMENS
SEPALS
A
PETALS
C
E
STAMENS
STAMENS
B-class expression in Musa explains monomorphic v. dimorphic perianth?
B/C-class expression in Ginger families explains ‘heterotopy’ in stamen whorl?
B
A
E
PETALS
STAMENS
Comparative analysis of gene expression:
B
A
PETALS
Wake, Wake & Specht 2011 Science
The ABC model of floral organ identity
SEPALS
Trend 2: Increase in perianth dimorphism
Petaloid
STAMENS
Petaloid
STAMENS
CARPELS
E
CARPELS
TEPALS
TEPALS
STAMENS
CARPELS
Tepals
Petals
Stamens
dimorphic
perianth
Carpels
TEPALS
www.weigelworld.com
B class MADS
box genes
TEPALS
STAMENS
STAMENS
CARPELS
(van Tunen et al. 1993
Kanno et al. 2007, Scientific World J )
DEFICIENS/APE
TALA3
GLOBOSA/PISTI
LLATA
B class genes & trait evolution
across monocots
1 GLO
1 DEF
2 GLO
1 DEF
3 GLO
2 DEF
Gene duplication
event
(~230-290 mya)
B
A
C
Ancestral B class
gene Kramer et al, 1998; Kim et al 2004
AP3/PI obligate heterodimers in Arabidopsis
DEF/GLO can homodimerize in monocots
1 GLO
4 DEF
Copy number?
Expression patterns?
Protein Function?
Kanno et al. 2007
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GLO-like
genes in the
Zingiberales
GLO-like
genes in the
Zingiberales
Copy number
Marantaceae
Cannaceae
Zingiberaceae
CostusGLO1
MusaGLO1
Costaceae
Marantaceae
Heliconiaceae
Cannaceae
Expression Pattern
Zingiberaceae
Strelitziaceae
Costaceae
Heliconiaceae
Lowiaceae
Strelitziaceae
Lowiaceae
Musaceae
Musaceae
Bartlett & Specht, 2010
Bartlett & Specht, 2010
GLO-like
genes in the
Zingiberales
DEF-like
genes in the
Zingiberales
CostusGLO1
MusaGLO1
Marantaceae
Two copies in all
families:
Zingiberalesspecific
duplication
Copy 1
Cannaceae
Zingiberaceae
Costaceae
Heliconiaceae
Strelitziaceae
Copy 2
Lowiaceae
Musaceae
CostusGLO2
A. Almeida, in prep
Bartlett & Specht, 2010
DEF-like
genes in the
Zingiberales
DEF-like
genes in the
Zingiberales
EXPRESSION:
Copy 2
SNP and
SPLICE
VARIATION
PHYML
aLRT
Copy 1
SEPAL
-
STAMEN
CsDEF2….
GYNOECIUM & LABELLUM
Copy 1
CsDEF2….
Copy 2
MuDEF2 same as MuGLO
A. Almeida, in prep
Copy 2
MuDEF2 same as MuGLO
A. Almeida, in prep
PHYML
aLRT
3
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DEF-like
genes in the
Zingiberales
Copy 1
SEPAL
-
Musa
STAMEN
ORGANSPECIFIC
Comparative MADS-box gene expression
Costus
MuDEF2
GYNOECIUM & LABELLUM
CsDEF2….
MuDEF2 same as MuGLO
CsDEF2
B-class
MuGLO
B-class
CsGLO2
CsGLO1
Copy 2
B
A
C
E
SEPALS
PETALS
STAMENS
CARPELS
PHYML
aLRT
A. Almeida, in prep
1 copy of AGL6
SEP-like genes in Monocots
SEP-like genes
in Zingiberales
Yockteng et al. 2013 MBE
SEP 3-like genes
2 copies in Zea
3 copies in Elaeis
2 copies in Oryza
2 copies of SEP3
SEP 1/2/4-like genes
= ‘LOFSEP’
5 copies in Zea
2 copies in Elaeis
3 copies in Oryza
AGL
6 1 copy
2 copies of LOFSEP
Zahn et al 2005, Malcomber & Kellogg 2005
Musa
Musa
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Organ Identity Genes ???
Primordia positioning
Primordia polarity
PHV
Organ Morphology Genes
PIN1
AUX1
LAX
PGP19
REV
AUXIN
Adaxial
PHB
ARFs
AXR1
AS1
KAN1-4
ARGOS
Margin
expansion
JAG
NUB
AGO1
Abaxial
YAB1-6
ANT
GA
CUC1-3
STM
CLV3
CK
CLV1
ARR
LFY
PAN
UFO
AG
WUS
AP1
AP3
AP2
PI
Primordia identity & growth
B
A
Petal
Sepal
SUP
C
Carpel
Stamen
Almeida et al. 2013 AoB PLANTS
Alvarez-Buylla et al. 2010 ‘the Arabidopsis book’
Polarity
• Laminar v. radial
Petaloidy
• Epidermal cell type
• Coloration pattern
Almeida et al. 2013 AoB PLANTS
Almeida et al. in review, Nature Reviews
Lamina outgrowth in the boundary
between adaxial and abaxial regions
Kidner and Timmermans CTDB 2010 91:141-168
(redrawn from Waites and Hudson 1995)
T
Polarity in leaves v. stamens
T
What is petaloid, anyway?
LUG
SEU
Toriba et al. 2011 Plant Signaling & Behavior
X
Ancestral=laminar
Musa
Costus
Canna
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Primordia positioning
PIN1
AUX1
LAX
PGP19
Primordia polarity
Abundant neg. reg. of HD-ZIPIII
Sakaguchi & Watanabe 2011
Dev Growth & Diff
REV
AUXIN
miR165/166
Adaxial
PHB
T
miR167
AXR1
ARFs
AS1
Polarity genes
Margin
expansion
JAG
NUB
KAN1-4
ARGOS
Polarity Gene Network
PHV
Arabidopsis
AGO1
Polarity and fertility of anthers/ovules;
Wu et al. 2006 Development
REV
Abaxial
YAB1-6
GA
STM
CLV3
CK
CLV1
ARR
LFY
UFO
AG
WUS
AP1
AP3
PI
Costus
comp25496_c0_seq1
10.9
6.125
GSMUA_Achr3G13970_001
comp25306_c0_seq1
Abaxial
LUG
SEU
19.13
2.645
GSMUA_Achr1G17950_001
comp33286_c0_seq1
13.82
GSMUA_Achr1G07120_001
comp33722_c0_seq1
4.81
7.365
10.06
30.745
GSMUA_Achr4G28360_001
comp13201_c0_seq1
1.675
2.075
GSMUA_Achr7G01060_001
comp13201_c0_seq1
0.51
2.075
GSMUA_Achr4G31660_001
comp13201_c0_seq1
7.195
2.075
GSMUA_Achr5G02420_001
comp28582_c0_seq1
2.13
GSMUA_Achr2G13050_001
comp13201_c0_seq1
0.785
2.075
GSMUA_Achr7G07830_001
comp33903_c0_seq1
97.8
91.995
GSMUA_Achr8G11580_001
comp29400_c0_seq1
11.26
4.14
GSMUA_Achr7G01330_001
YABBY2
(NM_001084021.1) GSMUA_Achr6G31080_001
YABBY5
GSMUA_Achr2G12850_001
(NM_179749.2)
comp35601_c0_seq1
395.8
15.675
comp36506_c0_seq1
66.69
65.05
comp35601_c0_seq1
14.7
15.675
GSMUA_Achr4G22750_001
comp35601_c0_seq1
26.65
15.675
KAN2
(NM_102957.3)
KAN3
(NM_117878.2)
Carpel
Alvarez-Buylla et al. 2010 ‘the Arabidopsis book’
5.98
3.32
comp38033_c0_seq1
GSMUA_Achr11G17520_001 comp29400_c0_seq1
ATS
GSMUA_Achr4G32400_001
(NM_001125891.1)
C
5.045
comp7486_c0_seq1
GSMUA_Achr9G03320_001
YABBY1 (AFO)
(NM_130082.3)
SUP
Stamen
Musa Costus
GSMUA_Achr5G29070_001
YABBY4 (INO)
(NM_102191.5)
Primordia identity & growth
B
A
Petal
AS1
(NM_129319.3)
PHB
(NM_129025.3)
REV
(NM_125462.3)
PHV
(NM_102785.4)
AGO1
YAB1-6
AP2
Sepal
Margin
expansion
KAN1-4
PAN
AGO1
(NM_1198240.1)
Adaxial
PHB
ANT
CUC1-3
Mean FPKM
Musa
GSMUA_Achr3G27070_001
PHV
2.19
4.41
4.14
comp4458_c0_seq1
1.185
3.42
GSMUA_Achr10G06430_001 comp30224_c0_seq1
16.44
5.495
GSMUA_Achr2G18070_001 comp33811_c0_seq1 4.265
8.03
Almeida et al. in review, Nature Reviews
Polarity Gene Network: radial v. laminar morphology
PHV
REV
Adaxial
PHB
YABBY 2/5
KAN1-4
AGO1
Abaxial
YAB1-6
KANADI• YABBY shows increase in expression
Almeida et al. in review, Nature Reviews
in radialized filament.
• Consistent with data from Arabidopsis
stamens.
• Indicates filament is abaxialized?
• There is no “stamen” gene – its
stamen morphology gene regulatory
network....
Almeida et al. in review, Nature Reviews
B
Fusion and Organ boundaries
Comparative MADS-box gene expression?
A
SEPALS
AS1
Musa
PHV
C
PETAL
S
STAME
NS
CARPE
LS
Costus
REV
PHB
Adaxial
AS1
MuDEF2
KAN1-4
AGO1
YAB1-6
CsDEF2
B-class
MuGLO
MuAG-2
Abaxial
CsGLO1
MuAG
C-class
CsAG-2
SEP3-1
FUSION:
• AS1 (MYB TF) gain of function results in
cotyledon fusion
• Functions to suppress CUC genes (NAC
TFs) which specify organ boundaries and
are important for organ separation
Koyama et al. 2010 Plant Cell
B-class
CsGLO2
CsAG-1
SEP3-2
SEP
LOFSEP1
LOFSEP2
AGL6
C-class
SEP3-1; SEP3-2
LOFSEP2
SEP
LOFSEP1LOFSEP1
AGL6
Yockteng et al. 2013 MBE (SEP)
Almeida et al. in prep (C-Class; DEF)
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Roxana Yockteng
Ana Almeida
Chodon Sass
Alma Pineyro-Nelson
Nisrine Machaka-Houri
Thiago Andre
Stephen Yee
Gracie Benson-Martin
Susan Hepp
Riva Bruenn
Kelsie Morioka
Molly Ng
Mechanisms of Developmental Processes underlying
organ-specific morphological diversification
SEPALS
PETALS
STAMENS
STAMENS
CARPELS
Katharine Yu, Cameron Messer,
Grady Pierroz, Olivia Cope
NSF - DEB & IOS (CAREER)
Undergraduate Research Apprenticeship Program (URAP)
Sponsored Projects for Undergraduate Research (SPUR)
UCB Committee on Research
UC MEXUS Collaborative Research Development Grant
Prytanean Alumni, UC Berkeley
Hellman Family Faculty Fund
Fulbright/CAPES
Wake, Wake & Specht 2011 Science
T
ancestral/laminar
LOFSEP
gingerspecific
duplication
T
Fertility and repression of laminar expansion?
Musa
LOFSEP
SEP3
gingerspecific
duplication
Duplication
Significant
change in
selection
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SEP3
Duplication
ZinSEP3-1
ZinSEP3-2
-Missing three amino acids in ZinSEP3-2
-located in the second α-helix of the K
domain.
-α-helices are important for protein-protein
interactions
Musa
AGL6 – 1 copy, lost ‘expressed everywhere’ pattern
SEP3 – consistent expression patterns, candidate for neofunctionalization
LOFSEP – variable expression, candidate for subfunctionalization
8