Light Perception Underground

Plants are divided into two parts. The shoots that gather light for photosynthesis and the roots that forage water, nitrogen, and other nutrients.

These are their stories.

If that sounds like the opening of Law & Order, that is because like the police and district attorneys in that series – shoots and roots – work independently and in concert with one other to conduct a plant’s business: optimizing photosynthesis, absorbing nutrients from the soil, and keeping those two roles in balance to successfully produce the next generation of plants. To do this, plants need to be able to sense light, water, and nutrients. Two 2016 studies found both indirect and direct ways that information about light, perceived by plants perceive in their shoot systems , is transmitted to the roots. They are among the newest discoveries in the story of how plants turn light into behavioral change, centering on a gene called HY5 discovered 37 years ago.

A suite of light sensors attuned to different colors of light (ultraviolet, red, blue, etc.) direct plant behavior. These sensors monitor ever–changing light conditions as sun and clouds track across the sky. Observing shifts in light adjusts plant behaviors from day to night. Light also tunes photosynthesis for sunny vs. cloudy days and other conditions. Plants take in carbon dioxide and use energy derived from light to split water molecules, building sugar and releasing oxygen. Sugars created in photosynthesis form the base of the food chain, making photosynthesis essential to life on Earth. Grains, meat, coffee, beer, wine, chocolate, air, and more are brought to you by photosynthesis.

While plants need sugar to build their bodies, other nutrients like nitrogen also make up the stuff of life. Most plants get these from the soil through their root systems. Plants need nitrogen and carbon to create molecules like DNA that make life, life. Combining carbon from photosynthetic leaves and nitrogen from the belowground roots requires moving them around the plant.  Once together, they are transformed in various ways to address plant cells’ needs. This is metabolism— managing and transforming molecules into useful forms. One example is the carbon-nitrogen compound caffeine people use as a stimulant.

Just as humans perk up with a cup of coffee as caffeine moves from stomach to brain, sending “wake-up!” signals head to toe, plants also circulate signals. In part, this balances sugar-making photosynthesis and nitrogen-absorbing root cells. Light sensors communicate with photosynthetic machinery to optimize its light harvesting activity and communicate with roots so they know what the shoot is doing. If photosynthetic sugar production is high, roots need to know to find and absorb more nitrogen too. This long distance, body-wide communication is why plants need to move information obtained from light underground. Both 2016 studies also help answer a previous observation made in plants, that light sensors are also present in roots that rarely, if ever, see the light.

HY5 is responsible for translating light into whole-plant behavioral changes. To understand why this gene is so central,  let’s start with the discovery of how plants see and process light in the first place.

How We Learned How Plants Interpret Light

Picture1

HY5 was discovered in 1980 by Maarten Koorneef at the Agricultural University in Wageningen, The Netherlands. Not much was known about the “machinery” plants used to govern their biological processes. What specific proteins sense and translate light into a biological response? Koorneef’s approach was akin to figuring out how a bicycle works by removing parts one at a time. Removing the pedals and riding it, you’ll quickly conclude that pedals aren’t essential, but not having them makes cycling challenging. He studied plant light responses by essentially removing individual protein-coding genes from the plants’ genome. He did this randomly and blindly, seeing only the outcome — a change in appearance in the light (Figure 1). He then did refined experiments (e.g. growing plants under only red light) to infer the possible role of the removed gene.

Koorneef identified five genes, labeled as HY1 through HY5, with changed light behavior. He proposed ideas for the roles of HY1–4 based on some experiments, but didn’t speculate about HY5.

In 1997, scientists at Kyoto University published that HY5 is a gene coding for a protein responsible for turning on and off other genes. Light perceived by a light sensor protein stabilizes HY5 protein. HY5 protein flips on or off specific genes to change plant behaviors, like initiating photosynthesis after a seed germinates and sees light for the first time. Plants lacking HY5 have a break in their biological wiring. The signal comes in, but information is not efficiently transmitted.

The Kyoto university team also reported a key observation the 2016 studies build on: that plants without a HY5 gene also had differences in their roots (Figure 2). They spread out wider rather than growing narrowly and down as normal roots do.

HY5 Moves From Shoot to Root and Roots Directly Sense Light

Light-activated HY5 protein moves from shoot to root. In the root it activates genes involved in bringing nitrogen from the soil into the root according to a report published in Current Biology last year from researchers at The Chinese Academy of Sciences and Oxford University. They observed that plants with illuminated shoots had more nitrogen than plants grown in the dark. This difference was not seen when roots were illuminated and shoots kept in the dark. They also observed that plants lacking HY5 did not absorb as much nitrogen. These results support the idea that the HY5 protein moves.

To catch HY5 moving from shoot to root, the scientists grafted a shoot with a marked version of HY5 onto roots and saw the marked HY5 show up in the root. Using a clever molecular biology approach, they also created a “bulky” version of HY5 that was stuck in illuminated shoots. When the bulk was clipped off the marked HY5 protein again showed up in roots. More light means more HY5 in roots and Picture1therefore more nitrogen in the plant.

Light itself actually moves through the shoot to the root too according to another paper published in Science Signaling by a consortium of Korean scientists. They also illuminated shoots while keeping roots in the dark, and found the expression of many genes in roots changed, among them, HY5.

“I think it is possible that stem-piped light controls nitrogen foraging through activating HY5 in the roots,” said lead author and postdoc Hyo-Jun Lee. Their data are consistent with the Current Biology study, even though they didn’t explicitly focus on nitrogen uptake. Instead, they observed an increase in HY5 in roots when shoots were kept in the dark for two days and then re-illuminated. HY5 is normally in roots, and the Science Signaling study shows that light in the shoots increases HY5 made by root cells. They convincingly show that the HY5 they detected originated in the root and is thus a second, direct, source of HY5 in roots.

Lee and colleagues also provide an explanation for plant light sensors being present in roots. One light sensor protein, phytochrome B (aka HY3), senses red light and stabilizes HY5. The researchers grafted shoots lacking phytochrome B onto roots with functional phytochrome B and vice-versa. Only plant roots with normally functioning phytochrome B had more HY5.

Some light perception in roots is thus required to produce and stabilize root HY5 protein. This direct light piped through shoots to the roots results in roots spreading out more, being less sensitive to gravity, perhaps signaling the root to seek nitrogen.

The Long Path to Understanding Light Signals in Roots

Plants increase HY5 protein in roots to signal that light is present. Both the indirect and direct routes of getting HY5 in roots cause changes in their behavior– to nitrogen uptake and gravity response, respectively. It is still unclear if these separate HY5 sources cause overlap in their influence on root behaviors.

If a plant is a house and each cell a room, Koorneef’s 1980 research partially drew back the curtains of a few windows to reveal how a plant translates perceived light into behavior. Koorneef said in his email that it was satisfying that the HY1–4 predictions made in his 1980 paper have been shown correct.

Thirty-seven years later, we know HY5 works in individual rooms and moves between them. The HY5 protein is a hub in a complex network of proteins communicating light and nutrition information to the basement of the house that doesn’t see much light. When roots do see light, HY5 protein appears there too. Plants are complex systems, and what we’ve learned about light responses in these studies likely applies to many plants, but likely not all ~400,000 known plant species.

Plants’ two systems, shoots and roots are a complex network of proteins, sugar, nutrients, photons, water, and more coursing between both to coordinate behavior. This coordination is why light goes underground. Plant cells act independently and as collective, like ant colonies. Plants’ complexity means adaptation, survival, and for us, life support. 

Ian Street, PhD is a plant scientist, freelance writer, and editor. His science blog is The Quiet Branches.

Image courtesy of Wikimedia Commons

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