Science - USA (2019-08-30)

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lower petal of some Mimulus flowers. The
red usually appears as a band of speckles,
which serve as a “nectar guide” for incom-
ing pollinators. Many types of coloration
in plants and animals are the result of a
network of proteins that activate pigment
genes at specific places and times in the
body. But Yuan and Blackman wondered
whether the monkeyflower spots might
be generated instead through a pattern-
ing mechanism proposed in the 1950s by
Turing, who is best known for breaking the
Germans’ Enigma code in World War II but
was also a theoretical biologist.
Turing predicted that some patterns
emerge from the natural diffusion and in-


teractions of proteins whose concentrations
regulate each other’s production. For spots,
when the gene encoding a cell’s “activator” of
pigment production turns on, the activator
protein stimulates its own production and
that of a “repressor” protein, which diffuses
beyond the pigmented spot. That second
molecule shuts down any activator in the
surrounding cells—causing a white halo. But
the repressor gets more dilute the farther it
travels, eventually losing its effect. Then the
activator can turn on, and a new spot of color
can form. Color patterns emerge depending
on the differences in the two proteins’ diffu-
sion rates (see diagram, below).
Biologists have long assumed that Turing’s

mechanism is responsible for zebra stripes
and leopard spots and perhaps even for
monkeyflower nectar guides. Indeed, Yuan
had identified a monkeyflower protein that
might serve as the activator. But no one had
identified a full activator-repressor system
involved in periodic pigmentation patterns.
Blackman, however, had noticed a clue in
some wild M. guttatus: They either lacked
spots or else had just one large red patch,
which he called a tongue, suggesting part
of the system was missing. Independently,
Yuan uncovered a similar red tongue variety
among mutants he made in another Mimu-
lus species. When they learned of each other’s
work, the two joined forces. And at the June
Mimulus meeting, they reported using the
red tongue varieties to track down a protein
dubbed R3-MYB, the repressor counterpart
to the already known activator protein.
To confirm that R3-MYB really acted as a
repressor, Yuan and Blackman both wielded
molecular tools to block its production.
Yuan relied on RNA interference, whereas
Blackman’s team enlisted CRISPR—the
first use of the genome-editing technology
in Mimulus. Both techniques led to full red
tongues on the plants’ petals, Blackman re-
ported—vivid testimony that the mechanism
Turing hypothesized can account for some
of nature’s tapestry. “This work shows how
Mimulus can provide broad insight into pro-
cesses that shape biodiversity,” Sweigart says.

ANOTHER LINE OF WORK with monkeyflow-
ers sheds light on biodiversity by revealing
a mechanism, unique to plants, for rapidly
adapting to new conditions. Their advan-
tage, graduate student Jaime Schwoch of
Portland State University in Oregon found,
is rooted in the way they produce reproduc-
tive cells. In animals, the cells that mature
into eggs and sperm are sequestered early
in development, and they don’t divide until
the organism sexually matures. That pro-
tects them from division-related mutations
that occur in the organism’s nongerm, or
somatic, tissues. But flowers, which con-
tain both kinds of germ cells—pollen and
ova—form from active somatic tissue at the
tips of growing stems. Any mutations oc-
curring in the dividing cells of a stem will
be locked into the germ cells and can pass
on to the next generation.
Given that somatic tissue mutations
should accumulate in a plant’s germ cells
over successive generations, Schwoch won-
dered why plants don’t wind up with many
more such mutations than animals—and
a greater burden of harmful ones. In fact,
as the somatic parts of both plants and
animals grow, their cells accumulate about
one mutation per million bases per cell di-
vision, so plant germ cells should have far CREDITS: (GRAPHIC) V. ALTOUNIAN/

SCIENCE

; (IMAGES) QIAOSHAN LIN AND BAOQING DING

Initial condition: high
concentration of activator
because of self-activation.
Activator difuses.

Pigment spot develops, but
inhibitor concentration grows
because of activator activity.

Activator levels decline at the
border of the spot because of
competition from faster-difusing
inhibitors. Spot is isolated.

Activator

Inhibitor

Concentration

Pigment
change
occurs

No change
in pigment
from default

Turing’s idea


takes root
Spots, stripes, and
monkeyflower petal
speckles arise through
“reaction-diffusion”
(top right), which
involves an activator
protein that turns on
pigment pathways and
the production of a
second protein, which
inhibits the activator.


Spot on
Unimpeded by the inhibitor, an activator colors a cell and spreads to and colors nearby cells. The inhibitor quickly
diffuses away from the colored cells, causing a nonpigmented halo to form. As this process repeats throughout the
tissue, multiple spots form, resulting in a periodic pattern.


Both the activator and the
inhibitor diffuse away from the
cells that produce them, with the
inhibitor moving faster (above).

The balance of concentrations
between the two proteins
determines whether pigment
is produced.

s o d m a a a o v

Patterns galore
Monkeyflower hybrids mix different species’ activators
and inhibitors, altering petal speckle patterns.


856 30 AUGUST 2019 • VOL 365 ISSUE 6456


Published by AAAS
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