Evolutionary and developmental

origins of leaves

Photo courtesy Tom Donald

 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

divideseveral
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 thedifferent 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

Cell division Patterning and Differentiation

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.
 In seed plants the shoot apical
meristem is multicellular
Cells in the central zone
are a pool of
undifferentiated stem cells Peripheral
Cells in the peripheral zone zone Central zone
proliferate and differentiate
into lateral organs

Cells in the rib meristem

proliferate and Rib
differentiation into the stem meristem
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

As a weak acid, IAA is a charged

Cell wall pH 5.5
anion(IAA)inthecytoplasm(pH7)
-

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+
 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
Thetinyleaves
that surround
the meristem
are called leaf
primordia

Arabidopsis thaliana

Nicotiana tabacum (tobacco)

SAM

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

Photo credit: Tom Donald

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 timesTracheophytes – 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 thesebryophytes
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

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

 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 orother 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