A team of biologists from UC San Diego, the Salk Institute for Biological
Studies and Oregon State University has identified the genes that enable
plants to undergo bursts of rhythmic growth at night and allow them to
compete when their leaves are shaded by other plants.
The researchers report in this week's issue of the journal PLoS Biology that
these genes control the complex interplay of plant growth hormones, plant
light sensors and circadian rhythms that permit plants to undergo rhythmic
growth spurts at specific times of the day or year in response to varying
levels of light and other environmental conditions.

Their discovery of the genetic underpinnings of the rhythmic plant movements
that enthralled Charles Darwin more than a century ago could eventually
allow scientists to design crops that can grow substantially faster and
produce more food than the most productive varieties today.

"This paper builds on our previous findings that almost all plant genes are
expressed only at a particular time of the day," said Howard Hughes Medical
Institute investigator Joanne Chory, a professor in the Salk Institute's
Plant Biology Laboratory.

"What we found is a whole raft of genes that could be the actual molecular
switches that define plant growth at the molecular level," said Steve Kay,
Dean of the Division of Biological Sciences at UC San Diego and one of the
leaders of the research team. "The more we understand about these genetic
mechanisms and how they switch on and off plant growth, the better we will
be at designing tailor-made crops to increase our production of food and
fuel for the world's rapidly growing population."

"It was known that the circadian clock confers an adaptive advantage to
plants in nature, and these findings provide a direct mechanism by which
plants optimize their growth by synchronizing hormone signaling with the
environment," said first-author Todd Michael, a former postdoctoral fellow
at Salk who is now an assistant professor of genomics and bioinformatics at
the Waksman Institute and Rutgers University. Other coauthors included UCSD
postdoctoral fellows Ghislain Breton and Samuel Hazen, and assistant
professor of genome biology, Todd Mockler, and graduate student Henry Priest
of Oregon State.

How plants grow to maximize their survival in different environments has
long fascinated biologists. In 1880, Charles Darwin published The Power of
Movement in Plants, one of his lesser-known books in which he describes his
studies on the manner by which different types of plants grow and move in
response to various stimuli.

While most people might assume that plants grow at a slow and steady rate
throughout the day and night, Darwin and others found that they grow in
regular nightly spurts, with plant stems elongating fastest in the hours
just before dawn. See video of soybean sprout growth at:
www.biology.ucsd.edu/scicomm/video/bigbeansprout.mov

"Plants actually grow rhythmically," said Kay. "Some plants, like sorghum,
have the ability to elongate a centimeter or more each night."

Why plants have evolved mechanisms to grow rhythmically at night or in the
hours just before dawn is a mystery. But a similar interplay of light
sensing, plant hormones and circadian rhythms that leads to a pronounced
rhythmic growth by plants during certain seasons and when shaded by other
plants has a clear survival value.

"Any plant that is growing is in a situation in which it has to compete with
the plants growing around it, so it has to develop ways in which it can
measure its environment to enable it to compete," said Kay. "Plant cells
have phytochromes, which are essentially shade detectors that measure the
ratio of different colors of light that can tell a plant whether it's a
cloudy day or whether it's being shaded by another plant. And being shaded
by another plant is bad news, because that plant is devouring all of the
right color of light for photosynthesis. If plants detect they're shaded,
they elicit growth hormones to elongate. You can see that in the extreme
when you leave something on your lawn and the grass around it has grown
taller."

To determine which genes control these rhythmic patterns of growth, the
research team turned to Arabidopsis thaliana, a tiny mustard plant used as a
laboratory model by plant geneticists. Because Arabidopsis, like many other
plants, grows fastest in the hours before dawn when exposed to day and night
cycles of light, the scientists sought to determine which of its genes were
being turned on during that period. Using DNA microarray chips, they were
able to test thousands of genes at a time to determine which ones were
active during that period.

"We did many hundreds of thousands of measurements," said Kay, "and then
asked what genes are rhythmically being turned on and are correlated with
this rhythmic growth pattern just prior to dawn? What we found was that a
whole bunch of genes all scattered around the Arabidopsis genome that deal
with hormone biosynthesis, hormone signaling and hormone metabolism are all
tightly correlated with rhythmic plant growth. This told us that this set of
genes could be the actual molecular signature that defines plant growth at
the molecular level."

The scientists said these disparate genes act together to regulate rhythmic
plant growth much like a gate with its hinges controlled by photoreceptors
and the biological clock?opening in the predawn hours to allow a wave of
multiple plant growth hormones to act within the cells, then closing the
gate to put the brakes on plant growth until the next 24-hour cycle.

"This temporal integration of hormone pathways allows plants to fine tune
phytohormone responses for seasonal and shade-appropriate growth
regulation," they write in their paper. "Many different plant hormone genes,
including genes for hormones that promote and antagonize growth, are
co-expressed at the time of day that plants grow," said Chory. "That such an
extensive gene regulatory module exists was quite a surprise."

To illustrate their model, the scientists attached a glowing enzyme,
luciferase, to the genes they identified as responsible for rhythmic growth
in Arabidopsis plants. As the plants go through their rhythmic growth phase,
the Arabidopsis plants glow on and off as genes that regulate the opening
and closing of the gate to plant hormones are activated, then deactivated.
See video with narration at: www.biology.ucsd.edu/scicomm/video/sprouts.mov

The scientists also discovered that most of the genes involved in this
rhythmic predawn growth have a DNA sequence in common, a master controller
that they dubbed the HUD element?for "Hormone Up at Dawn." This HUD element,
they noted, must have a protein that attaches to it that regulates its
function.

"We don't know what that is, because we haven't found it yet," said Kay.
"Identifying that protein regulator is going to be a key goal for the future
because that protein is going to be very, very important for controlling
plant growth and yield."

"It's a very exciting time for biologists," Chory added, "because the tools
now exist to answer questions about complex processes, such as how plants
grow or how human metabolism goes awry."
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