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Secrets of the Plant "Intranet" Are Coming to Light

You've got mail.jpg

Most companies are on the Internet these days, but many also keep an internal network called an "intranet" for passing messages within the organization. In both respects, flowering plants and conifers are similarly equipped. They send and receive messages through the air in the form of volatile organic compounds, and through the soil by networks of fungal hyphae. A tree under attack by beetles, for instance, can send out distress calls that other trees in the forest can pick up, giving them time to shore up their defenses.

The plant "intranet" is where things really get interesting. When you think about it, a plant has to keep in touch with itself. The roots underground need to know how things are going up top. The leaves and branches, in turn, need to know if there will be enough water and nutrients in the soil to proceed with costly enterprises like flowering and fruit bearing. Plants have a remarkable communications system that allows rapid signaling and response, comparable to an automated email system.

The messages come in the form of molecules that travel through the vascular bundles in the stems and roots. A paper in Current Biology by Chinese scientists explains part of what happens. In effect, they opened a plant's email and read it. The message was in the form of a transcription factor named HY5, a protein that binds to a gene and controls its transcription rate. Wikigenes says that HY5 "binds directly to the promoters of light-inducible genes, promoting their expression and photomorphogenic development." The email says, "Turn up the heat, guys -- the economy is booming!"

But HY5 should not turn up the heat if the roots aren't ready in the supply room down below. Here's where long-distance communication comes in (long distance, that is, in the context of a small plant). The Chinese researchers found that HY5 migrates from the shoot to the root with its message. They list these four highlights of their findings:

  • HY5 is essential for light-responsive coordination of the growth of shoots and roots.

  • Shoot-to-root translocated HY5 mediate light-activated root growth and N uptake.

  • Carbohydrate photosynthate-induced NRT2.1 expression and N uptake depend upon HY5.

  • HY5 contributes to maintain balance of C and N metabolism at varying light fluence. [Emphasis added.]

Did you catch that word "translocated"? That's the email system. HY5 travels down the plant's phloem vessels from "shoot to root" -- from top to bottom. Watch for the intranet analogy in the summary of the paper. (Gene names are italicized; protein names are not.)

Coordination of shoot photosynthetic carbon fixation with root inorganic nitrogen uptake optimizes plant performance in a fluctuating environment. However, the molecular basis of this long-distance shoot-root coordination is little understood. Here we show that Arabidopsis ELONGATED HYPOCOTYL5 (HY5), a bZIP transcription factor that regulates growth in response to light, is a shoot-to-root mobile signal that mediates light promotion of root growth and nitrate uptake. Shoot-derived HY5 auto-activates root HY5 and also promotes root nitrate uptake by activating NRT2.1, a gene encoding a high-affinity nitrate transporter. In the shoot, HY5 promotes carbon assimilation and translocation, whereas in the root, HY5 activation of NRT2.1 expression and nitrate uptake is potentiated by increased carbon photoassimilate (sucrose) levels. We further show that HY5 function is fluence-rate modulated and enables homeostatic maintenance of carbon-nitrogen balance in different light environments. Thus, mobile HY5 coordinates light-responsive carbon and nitrogen metabolism, and hence shoot and root growth, in a whole-organismal response to ambient light fluctuations.

The key to any intranet is movement of information-bearing signals. In human email systems, each message has a "header" of metadata signifying the sender and receiver and other information, so that the router on the communications channel knows what to do with it. Then there is the body of the message. The plant's messages, of course, are different from human email written in alphabetic text; they're more like signals indicating "on/off" or "speed up/slow down." They are encoded, though, by molecular text -- the language of DNA. Notice that there's nothing about HY5 that looks like or smells like the meaning of the message. The meaning involves a pre-ordained convention about what the presence of the signal indicates.

It's notable that the same signal can take on different meanings depending on context. The signal causes one reaction in the shoot, but a different reaction in the root. We also see a "To" and "CC" convention. HY5 lands on two genes: HY5 and NRT2.1. There's a unique aspect of this plant intranet in that it's "fluence-rate modulated," i.e., sensitive to message flow: the more signal, the more the response. Maybe that's like getting a flood of tweets.

Most importantly, the message is mobile and routable. HY5 has to carry its message over long distances and traverse numerous branching points to get to the intended recipient. As a result, just as with a corporate intranet, the plant benefits from "whole- organismal response" to what we might call the business environment. Just as a manufacturing plant needs to adjust its production to the availability of raw materials, a living plant must adjust its production to the availability of sunlight and soil nutrients.

The paper reads like a detective story. When they shined light of varying intensities on shoots, the roots grew. Intrigued by the rapid response of a distant part of the plant to the conditions at the top, they thought, Aha! -- "Shoot illumination promotes root growth, most likely via shoot-to-root signaling." It's no wonder that in the introduction to the paper, the scientists described it as "long-distance shoot-root communication." The hunt was on to find the emails.

Experiments honed in on the answer. Mutant plants that didn't grow stronger roots when illuminated were found to have a broken HY5 protein. Other tests confirmed that HY5 is the information-carrying molecule. But does it really travel long distance? To test that, they ran some experiments that first suggested "HY5 transcripts, HY5, or a HY5-dependent signal moves from shoot to root." Then they narrowed it down to HY5 itself. One clever test was fastening two other molecules onto HY5 in the shoots, and finding that none of them made it to the root. Why? "Most likely because its relatively large size prevents shoot-root mobility" -- i.e., the bigger emails clogged the communication channel.

But then, when they sent along a molecular scissors that cut off one of the hangers-on, the custom messages did arrive. Conclusion: "HY5 is a shoot-root phloem-mobile signal...." From there, they studied what the recipient of the "CC" email does (i.e., the gene NRT2.1). The second recipient, they found, promotes a gene that increases nitrate uptake.

In the conclusion, the authors recognized that what they were seeing was a case of real communications networking. The shoot is not just sending some sugar down the pipe for the roots to eat so they will work harder; sucrose is involved, but the HY5 protein transcription factor is a bearer of information. Here's how they express it in scientific jargon:

Although a previous study implicates phloem-mobile sucrose as a cotyledon-derived signal to control primary root elongation during early seedling development in Arabidopsis, the molecular mechanism of the shoot-root long-distance signaling regulating lateral root growth and N uptake remains unclear. Here, we show that HY5 is a shoot-root mobile signal that mediates light-regulated coupling of shoot growth and C assimilation with root growth and N uptake. This coupling is achieved via HY5 regulation of C fixation in the shoot and via sucrose-enhanced promotion of HY5-dependent N uptake in the root. In consequence, HY5 mediates homeostatic regulation of whole-plant C versus whole-plant N status. HY5 is already known to integrate multiple phytohormonal (e.g., abscisic acid) and environmental (e.g., low temperature) signaling inputs in the control of plant growth and development. Our discovery that HY5 is a mobile signal adds further dimension to this knowledge.

This is so cool; everyone should get a chill out of thinking that plants have email. They pass signals coded by a genetic language. They send them through communications channels to recipients. The recipients know what to do with that information. The resemblance to email is uncanny. When ID advocates see very similar concepts to email employed in living organisms like the humble rockcress, we have ample justification to celebrate. "You've got mail!"

Image credit: © tobyc515 / Dollar Photo Club.