Evolutionary and developmental

origins of leaves

Photo courtesy Tom Donald

 Lecture outline
Evolutionary origins of leaves
Developmental origins of leaves
Structure and function of the shoot apical meristem
Experimental studies of phyllotaxy
Roles of auxin, auxin transport and biophysical forces
Mechanical signals and computer simulations

Photo courtesy Tom Donald

 What is a leaf?
Leaves are:
• Lateral outgrowths of a
plant shoot
• Usually determinate
(finite growth)
• Vascularized
• Initiated by the shoot
apical meristem
• Usually photosynthetic

Photo credit: Tom Donald

Evolutionary origins of leaves

Photo credits: Ghedoghedo, Tohoku University, Bolton Museum

Earliest land
plants
~ 425 million
years ago

Leaves formed in the Flowers formed in the

Devonian period ~ 360 - 400 Cretaceous period ~ 130
million years ago million years ago

The Evolution of Plant Architecture (original by A. R. Hemsley).

The earliest land plants did not
produce leaves

Cooksonia and Rhynia lived

about 400 million years ago

Image credits: Ville Koistinen; Griensteidle

Leaves have evolved independently
multiple times
Tracheophytes – vascular plants

Bryophytes
Euphyllophytes
– mosses, Lycopods
liverworts – club Ferns Gymnosperms Angiosperms
mosses

Rhyniophytes
(extinct)

Redrawn from Tomescu, A.M.F. (2009) Megaphylls, microphylls and the evolution of leaf development. Trends Plant Sci. 14: 5–12.
Non-vascular plants do not have
leaves
The leaf-like structures
on these bryophytes
are not true leaves.

B L F G A

Image credit: tom donald; encyclopetey; Jesse Hickman

 Early leaves were little more than
flaps of tissue

Lycopodium and
Selaginella have
leaves that
resemble the
earliest leaves

Image credits: Vzb83; tom donald; Luis Fernández García

 Lycopod leaves

• Small, single vein

• “Microphylls”
• Resemble early leaves

B L F G A

Image credit: tom donald

Larger and more complex leaves
evolved in ferns and seed plants

Image credit: tom donald

Leaves are derived from modified
branches

Leaves provide
increased surface area
for light harvesting and
CO2 uptake for
photosynthesis

Reprinted by permission from Macmillan Publishing Ltd: Kenrick, P. (2001). Palaeontology: Turning over a new leaf. Nature 410: 309-310 copyright 2001.
Leaves are renewable resources

In many plants, leaves are

short-lived organs that can
be replaced annually or if
they are damaged.
Often leaves open in the spring.
The green, nitrogen-rich chlorophyll
is degraded and the nutrients
reabsorbed before the leaves are
dropped in the autumn

Photos by Tom Donald

 Fern leaves

B L F G A

Image credit: tom donald

Photos courtesy of tom donald

 Gymnosperm leaves

Dioon

Pinus Welwitschia

B L F G A

Ginkgo
Gnetum
Image credits: BotBln; MPF; Muriel Gottrop; James Field ; Daderot

Photos courtesy of tom donald

 Angiosperm leaves

B L F G A

Image credit: tom donald

Photos courtesy of tom donald

 Developmental origins of leaves

How are living

structures formed?
How are patterns
initiated, stabilized
and elaborated,
over and over and
over again?
 How to build an organism

Start with a
single cell
(usually a zygote
resulting from
the fertilization
of an egg by a
sperm)
 How to build an organism

Cell division

Let that cell

divide several
times
How to build an organism
Introduce
variation – make
the cells unequal
This can be a
very localized
change

Or a gradual,
gradient-like
change
How to build an organism
Let the different They can
cells behave divide more
differently

or they can
grow more
 Plants and animals both start out as
a single cell

Zygote Zygote

Embryonic Embryonic
development development
 The same principles underlie early
development in animals and plants

zygote

Patterning and Differentiation

Cell division
organogenesis and growth

zygote
Animals are small but fully formed at
the end of embryogenesis
Plants continually make new organs
as they grow – leaves, roots, flowers
Post-embryonic organ formation occurs
through the action of meristems
Shoot
apical
meristem

Embryonic development of Arabidopsis

Root apical meristem

Capron, A., Chatfield, S., Provart, N., and Berleth, T. (November 12, 2009) Embryogenesis: Pattern Formation from a Single Cell. In The Arabidopsis Book, CR.
Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10/1199/tab0129.
 The shoot apical
meristem makes the
stem, leaves, flowers
fruit and seeds

The root apical

meristem makes
the primary and
lateral roots
 The shoot is made up of repeating
units called phytomers
A phytomer consists of a leaf, a node,
an internode and an axillary meristem

SAM

LEAF
INTER-
AXILLARY NODE
BUD
NODE
AXILLARY NODE
INTER- BUD
NODE

The lower part of a grass leaf, the

sheath, wraps around the stem
Adapted from Sanchez, P., Nehlin, L. and Greb, T. (2012). From thin to thick: major transitions during stem development. Trends Plant Sci. 17: 113-121. Forster, B.P., Franckowiak, J.D., Lundqvist, U., Lyon,
J., Pitkethly, I. and Thomas, W.T.B. (2007). The Barley Phytomer. Ann. Bot. 100: 725-733. Tsiantis, M. and Hay, A. (2003). Comparative plant development: the time of the leaf? Nat Rev Genet. 4: 169-180.
 The shoot apical meristem is tiny
and usually hidden from view
SAM SAM
The tiny leaves
that surround
the meristem
are called leaf
primordia

Arabidopsis thaliana

SAM
Nicotiana tabacum (tobacco)

The meristem is usually

0.1 – 1 mm in diameter

Oryza sativa (rice)

 The shoot apex of ferns is
dominated by a single apical cell
The apical cell (A) cleaves off alternating faces when dividing, retaining its shape

A A A

A A

Redrawn from Golub, S.J., and Wetmore, R.H. (1948) Am. J. Bot. 35: 755-767.
 In seed plants the shoot apical
meristem is multicellular
Cells in the central zone
are a pool of
undifferentiated stem cells Peripheral
zone Central zone
Cells in the peripheral zone
proliferate and differentiate
into lateral organs

Cells in the rib meristem

proliferate and Rib
differentiation into the stem meristem
One of the functions of the shoot
apical meristem is to make leaves
 Leaves are lateral organs that derive
from founder cells
1. Cells at the periphery of
the SAM are specified to
adopt a different fate to
surrounding cells Specification

2. This process gives rise Founder cell

to leaf founder cells that (organ initial)
are morphologically
indistinguishable from the Activation
Increasing:
surrounding cells
Leaf • Cell number
primordium • Cell differentiation
3. Activation of founder
cells involves subsequent Growth and
cell divisions to create a differentiation
primordium that will
develop into a leaf Leaf
Adapted from Moon, J. and Hake, S. (2011). How a leaf gets its shape. Curr. Opin. Plant Biol. 14: 24-30.
 Sector analysis reveals number of
leaf founder cells
Leaf Leaf Arabidopsis sector
Half albino Mostly albino analysis

Juniper leaves
showing albino SAM SAM
partial sectors (ps)
and entire sectors
(es). The number of
leaf founder cells
can be calculated
Founder Founder
from the smallest
sector unit
population population
half albino mostly albino
Reprinted with permission from Korn, R.W. (2002). Chimeric patterns in Juniperus chinensis ‘Torulosa Variegata’ (Cupressaceae) expressed during leaf and stem formation. Am. J. Bot. 89: 758-765.; Irish, V.F. and Sussex, I.M. (1992). A
fate map of the Arabidopsis embryonic shoot apical meristem. Development. 115: [Link] also Poethig, R.S. and Sussex, I.M. (1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165: 170–184.
 Phyllotaxy

Phyllotaxy is the pattern of organ initiation at the shoot apical meristem

Alternate Opposite Whorled Spiral

 Alternate phyllotaxy

SAM

Cross section of maize apex

One leaf at a time, as in

rice or other grasses
Candela, H. Johnston, R., Gerhold, A., Foster, T., and Hake, S. (2008) The milkweed pod1 gene encodes a KANADI protein that Is required for abaxial/adaxial patterning
in maize leaves. Plant Cell 20: 2073-2087; Itoh, J.-I., Kitano, H., Matsuoka, M., and Nagato, Y. (2000) SHOOT ORGANIZATION genes regulate shoot apical meristem
organization and the pattern of leaf rrimordium initiation in rice. Plant Cell 12:2161-2174
Opposite phyllotaxy

Two at a time, 180° apart

at each node. Sometimes
pairs alternate by 90° at
successive nodes

Image credit: Juni

 Whorled phyllotaxy

Three or more leaves at

each node, as in Galium
odoratum
Photos courtesy of James Lindsey and Jopi
 Spiral phyllotaxy

In most plants,
such as this
succulent,
leaves form in
a regular spiral
pattern
Photos courtesy of tom donald
 Spiral phyllotaxy

In plants with spiral

phyllotaxy, leaves
form at about
137.5° apart

137.5°
The angle of leaf placement dissects
the apex by the golden ratio

360 222.5
137.5° = 1.618 =
222.5 137.5
360° 222.5°
The golden ratio is visually pleasing
and used by artists and architects
The lengths of the
Golden Rectangle sides differ by the
golden ratio
Spiral phyllotaxy
Spiral phyllotaxy
Spiral phyllotaxy
 Spiral phyllotaxy

A line through
sequential
leaves makes a
spiral
 Spiral phyllotaxy

The NEXT leaf

to form is called
the Incipient
primordium (I1)
I1
 Spiral phyllotaxy

The one that will

form after that is
called I2….etc.

I1
I2
 Spiral phyllotaxy in tobacco apex

I1

Reprinted from Poethig , R.S. and Sussex ,I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: 158-169 with kind permission of Springer Science+Business Media.
 What determines the placement of a
new leaf?

•Chemical inhibitor?
•Competition for an
activator?
•Physical forces?
What determines the position of the
incipient leaf primordium?

Surgical experiments
demonstrate that leaf
placement is
determined by pre-
existing primordia

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 I2

This tomato apex shows the positions of several

primordia (P) and incipient primordia (I)

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

I1

P1

I2
P2 I2

This tomato apex shows the positions of several

primordia (P) and incipient primordia (I)

The expected position for I3 (*) can be found by

tracing the spiral
Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

I1

P1

P2 I2

I1 (shown in black) was

surgically isolated from
the rest of the meristem,
by cutting along the red
line
Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

Two days later, the apex

I1 was examined

P1
P2
I2

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

I3 Instead of emerging at its

I1 expected position (star), I3
shifted towards I1

P1 This experiment shows

P2
that I1 influences I3
I2
position

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

I3
I1

P1
P2
I2

Positions of I2 and I3;

older leaves have been
cut away

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 P3

I3
I1

P1 The older primordia control

P2
I2 the placement of the incipient
primordia

What kind of signal or information is involved?

Reinhardt, D., Frenz, M., Mandel, T., and Kuhlemeier, C. (2005) Microsurgical and laser ablation analysis of leaf
positioning and dorsoventral patterning in tomato. Development 132: 15-26. Reproduced with permission.
 Studies suggested an inhibitor or
competition for activator was involved

Experimental studies suggested P5

that leaf primordia are surrounded I1
by zones of inhibition in which new P3
primordia cannot form
P2 M
These zones could be caused by
production of an activator, or I2 P1 P6
depletion of an inhibitor P7
P4

Adapted from Wardlaw, C.W. (1949) Experiments on organogensis in ferms. Growth (Suppl) 13: 93 0 131 as cited in Steeves and Sussex.
 Phyllotactic patterns are disrupted
in mutants with enlarged meristems
Mutants of Arabidopsis and
Zea mays with enlarged
meristems

Wild-type clavata1
Wild-type abphpyl1
spiral random
alternate opposite
Reproduced with permission from Clark, S.E., Running, M.P., and Meyerowitz, E.M. (1993). CLAVATA1, a regulator of meristem and flower development in
Arabidopsis. Development 119: 397-418. Jackson, D., and Hake, S. (1999). Control of phyllotaxy in maize by the abphyl1 gene. Development 126: 315-323.
Recent studies have indicated that
auxin is an activator for initiation

Indole-3-acetic acid (IAA)

a naturally occurring auxin Auxin accumulation
precedes leaf initiation
 Auxin transport is necessary for
primordium initiation

meristem

The apex of the

pin1 mutant is
bare – it fails to
produce lateral
organs. PIN1 is
an auxin efflux
carrier protein
Wild-type Arabidopsis pin1 shoot apex
shoot apex
Reprinted from Current Opinion in Plant Biology, 8 (1), Byrne, M.E., Networks in leaf development , 59-66, Copyright
(2005), with permission from Elsevier doi:10.1016/[Link].2004.11.009; Reinhardt D., Mandel, T., and Kuhlemeier , C. (2000)
Auxin regulates the initiation and radial position of plant lateral organs Plant Cell 12: 507- 518
 Auxin transport

As a weak acid, IAA is a charged

Cell wall pH 5.5
anion (IAA-) in the cytoplasm (pH 7)
Cytoplasm pH 7
In the more acidic cell wall (pH 5.5)
some is uncharged (IAAH). Thus IAA
can easily move into but not out of IAA-
cells
IAAH IAA- + H+

IAAH

IAA- + H+
 Auxin transport

As a weak acid, IAA is a charged

Cell wall pH 5.5
anion (IAA-) in the cytoplasm (pH 7)
Cytoplasm pH 7
In the more acidic cell wall (pH 5.5)
some is uncharged (IAAH). Thus IAA
can easily move into but not out of IAA-
cells
IAAH IAA- + H+
The PIN1 protein is an auxin efflux
carrier, transporting charged auxin
back out of the cytoplasm IAAH

IAA- + H+
 Auxin transport
Net flow
As a weak acid, IAA is a charged of auxin
Cell wall pH 5.5
anion (IAA-) in the cytoplasm (pH 7)
Cytoplasm pH 7
In the more acidic cell wall (pH 5.5)
some is uncharged (IAAH). Thus IAA
can easily move into but not out of IAA-
cells
IAAH IAA- + H+
The PIN1 protein is an auxin efflux
carrier, transporting charged auxin
back out of the cytoplasm IAAH

The distribution of PIN1 protein IAA- + H+

controls the flow of auxin
A local auxin maximum is required
for organogenesis
38 hours after application

Applying a spot of
exogenous auxin
(shown as a red
blob) stimulates
outgrowth of
primordium in the
pin1 mutant

Reinhardt D., Mandel, T., and Kuhlemeier , C. (2000) Auxin regulates the initiation and radial position of plant lateral organs Plant Cell 12: 507- 518.
A local auxin maximum is required
for organogenesis
38 hours after application 4 days after application

Reinhardt D., Mandel, T., and Kuhlemeier , C. (2000) Auxin regulates the initiation and radial position of plant lateral organs Plant Cell 12: 507- 518.
Auxin transport and accumulation
contribute to organ initiation
Cell wall pH 5.5
This conclusion is
supported by imaging
Cytoplasm pH 7
PIN1 distribution in
living plants
IAA-

IAAH IAA- + H+

IAAH

IAA- + H+

Reinhardt D., Mandel, T., and Kuhlemeier , C. (2000) Auxin regulates the initiation and radial position of plant lateral organs Plant Cell 12: 507- 518.
 Visualizing PIN1 localization

Emitted light

GFP

PIN1
GFP
Excitatory light

Green fluorescent protein A protein’s position within a

(GFP) emits green light cell can be determined by
when excited by blue light making a fusion protein of it
with GFP, and then looking for
GFP fluorescence
 Visualizing PIN1 localization

Reporter gene
in the nucleus

PIN1pro PIN1 GFP

mRNA

PIN1
GFP

Translation
PIN1

Fusion protein GFP

PIN1
GFP
Insertion into
membrane
 Visualizing PIN1 localization
Using a confocal laser
scanning microscope,
PIN1:GFP protein distribution
can be imaged in the shoot
apical meristem. In this image,
the green lines show the
position of PIN1:GFP at cell
membranes

PIN1pro

PIN1
PIN1 GFP GFP

mRNA
Reproduced with permission - Development Gordon, S.P., Heisler, M.G., Reddy, G.V., Ohno, C., Das, P., Meyerowitz, E.M. Development, 2007, 134 (19): 3539-3548.
PIN1 distribution is dynamic during
organogenesis

PIN1:GFP Positions of primordia

and incipient primordia

Reprinted from Current Biology 15: Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A., and
Meyerowitz, E.M. Patterns of auxin transport and gene expression during primordium development revealed by live
imaging of the Arabidopsis inflorescence meristem, 1899-1911, Copyright (2005), with permission from Elsevier.
The orientation of PIN1 within cells is shown
by white arrows, and indicates auxin flow
Reprinted from Current Biology 15: Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A., and
Meyerowitz, E.M. Patterns of auxin transport and gene expression during primordium development revealed by live
imaging of the Arabidopsis inflorescence meristem, 1899-1911, Copyright (2005), with permission from Elsevier.
 Auxin accumulates at I1 position

Reprinted from Current Biology 15: Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A., and
Meyerowitz, E.M. Patterns of auxin transport and gene expression during primordium development revealed by live
imaging of the Arabidopsis inflorescence meristem, 1899-1911, Copyright (2005), with permission from Elsevier.
The polarity of PIN1 protein forms an
auxin maximum at I1

I1
The polarity of PIN1 protein forms an
auxin maximum at I1

I1

This observation is
consistent with the
emergence of a
primordium at the site
of auxin application
 A subsequent reversal in PIN1
polarity changes the position of the
auxin maximum, specifying the site
of the next primordium

P3 P3
P1 P1

I1 I1
I2

P2 time P2
 After primordium initiation, PIN1
distribution changes, directing auxin
flow into the developing midvein
P1
I1
P1
I1

P1
I1
TIME

Poethig , R.S. and Sussex ,I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: 158-169. Figure 3 Copyright (1985) Planta.
Reprinted with kind permission of Springer Science+Business Media. Adapted by permission from Macmillan Publishers, Ltd: Nature Reinhardt D., Pesce, E.-R., Stieger, P.,
Mandel, T., Baltensperger, K., Bennett, M., Trass, J., Friml, J., Kuhlemeier, C. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255-260; copyright (2003).
 The auxin transport model can
generate a pattern de novo
Peaks of auxin time
accumulate in a
computer
simulation

Peak spacing
can be
The patterns that changed by
emerge resemble decreasing or
leaf formation increasing rate
(red represents PIN1
and lighter green is of transport
more auxin)

Smith, R.S., Guyomarc'h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C., and Prusinkiewicz, P. (2006). A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA 103:
1301-1306, copyright 2006 National Academy of Sciences, USA.
A time sequence of the model looks
like a real shoot apex

The simulation starts

from a radially symmetric
embryo, produces
opposite cotyledons, and
then settles into a spiral

Link to movie

Smith, R.S., Guyomarc'h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C., and Prusinkiewicz, P. (2006). A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA 103:
1301-1306, copyright 2006 National Academy of Sciences, USA.
What about plants with other
phyllotactic patterns?

Spiral Alternate
 Leaf initiation in monocots
In monocots such as corn (Zea mays),
leaves are initiated somewhat lower on
the meristem, and are derived from a ring
of cells around the meristem.

Scanlon, M.J. (2003) The polar auxin transport inhibitor n-1-naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol. 133: 597-605
 Inhibitors of polar auxin transport
prevent leaf initiation in maize

Maize plants were treated with a

Control polar auxin transport inhibitor
after the initiation of Leaf 5

In the control plants, after 14 days,

three more leaves were initiated (6, 7
and 8)

Scanlon, M.J. (2003) The polar auxin transport inhibitor n-1-naphthylphthalamic acid disrupts leaf
initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol. 133:
597-605
 Inhibitors of polar auxin transport
prevent leaf initiation in maize

Control

Transport
inhibitor In the plants treated with the
treatment auxin transport inhibitor, no
additional leaves were initiated

Scanlon, M.J. (2003) The polar auxin transport inhibitor n-1-naphthylphthalamic acid disrupts leaf
initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol. 133:
597-605
Polar auxin transport is required for organogenesis in
monocots and dicots, and in plants with spiral or
alternate patterns of phyllotaxy
 A role for cell stress and microtubule
orientation in primordia initiation
The cortical microtubule
array in plant cells is
dynamic and correlated Direction
with growth direction of growth

Directional array
correlated with Microtubule arrays
Random array unidirectional cell in Arabidopsis root
correlated with uniform expansion epidermal cells
cell expansion
Sugimoto, K., Himmelspach, R., Williamson, R.E., and Wasteneys, G.O. (2003). Mutation or drug-dependent microtubule disruption
causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root Cells. Plant Cell 15: 1414-1429.
Microtubule orientation is correlated
with stress orientation

At the apex stress is

isotropic (same in every
direction) and microtubule
orientation is random

At the crease between the

apex and primordium the
stress is strongly direction
as is microtubule orientation

From Hamant, O., Heisler, M.G., Jönsson, H., Krupinski, P., Uyttewaal, M., Bokov, P., Corson, F., Sahlin, P., Boudaoud, A., Meyerowitz, E.M., Couder, Y., and
Traas, J. (2008). Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655. Reprinted by permission from AAAS.
 Microtubules respond to changes in
pressure in adjacent cells
Before cell ablation – After cell ablation –
microtubule orientation microtubules reorient
random parallel to the change

Simulation

Experimental result

From Hamant, O., Heisler, M.G., Jönsson, H., Krupinski, P., Uyttewaal, M., Bokov, P., Corson, F., Sahlin, P., Boudaoud, A., Meyerowitz, E.M., Couder, Y., and
Traas, J. (2008). Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655. Reprinted by permission from AAAS.
 PIN1 polarity is correlated with
microtubule orientation

Cells in the boundary domain

In most cells the showing strong polarity of
orientation of PIN1 (red) is microtubules and PIN1
along a cell surface
parallel to the orientation
of microtubules (green)

Heisler, M.G., Hamant, O, Krupinski, P., Uyttewaal, M., Ohno, C., Jönsson, H., Traas, J., and Meyerowitz, E.M. (2010) Alignment between PIN1 polarity and
microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8(10): e1000516.
PIN1 moves away from ablated cells
Ablated cells

PIN1 on “away” surface

Microtubules

Heisler, M.G., Hamant, O, Krupinski, P., Uyttewaal, M., Ohno, C., Jönsson, H., Traas, J., and Meyerowitz, E.M. (2010) Alignment between PIN1 polarity and
microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8(10): e1000516.
 These studies suggest a model in
which PIN1 orientation responds to
cell pressure

Cell on right has PIN1 moves

towards that cell, Auxin-induced
increased internal
auxin flows in cell growth leads
pressure
to increased
internal pressure

Positive feedback loop

 Ongoing studies
How do microtubules
and PIN1 perceive and
respond to stress?

What controls different

phyllotactic patterns including
those of non-seed plants?

How did leaves contribute to the

ancient atmosphere and vice versa?

How do light and other

hormones feed into
phyllotactic patterning?
 Summary

• Multiple evolutionary origins for leaves

• Leaves form in regular patterns at the
shoot apex, often as a spiral
• Leaf initiation is determined in part by
auxin distribution and PIN1
• Primordia affect placement of incipient
primordia, possibly through biophysical
effects
• Computer simulations can recreate
phyllotactic patterns and test hypotheses