Vegetative Warfare | January 31, 2011 Issue - Vol. 89 Issue 5 | Chemical & Engineering News
Volume 89 Issue 5 | pp. 53-55
Issue Date: January 31, 2011

Vegetative Warfare

Plants have evolved sophisticated weaponry to battle bacterial and fungal invaders
Department: Science & Technology
Keywords: Plant immunity, microbes, fungi, bacteria
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EXPANDING PREDATOR
Wheat stem rust first originated in Uganda, but the fungus has since devastated crops as far away as Iran.
Credit: USDA-ARS Cereal Disease Laboratory
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EXPANDING PREDATOR
Wheat stem rust first originated in Uganda, but the fungus has since devastated crops as far away as Iran.
Credit: USDA-ARS Cereal Disease Laboratory

Plants don’t get a fever when they’re sick from a microbial pathogen. Nor do they dispatch an army of white blood cells to the point of infection—in fact, plants don’t have any circulating cells at all. But this doesn’t mean plants don’t have a battery of cunning defense measures that they use to protect themselves from invading bacteria, fungi, and other pathogens.

Over the past decade or two, researchers have figured out that plants have two major protection strategies. The first response is an array of molecules that recognize and suppress alien organisms. The second strategy involves a sequence of arms-race operatives against pathogens that outwit the first responders.

Much of what we know about the complex architecture of a plant’s immune system has come from genetic techniques and genomics. But as researchers begin to tackle the molecular mechanisms that plants use to wage war, leading plant immunity researchers are calling for more experts in biochemistry, proteomics, and structural biology to help tease out the tricks that plants use to protect themselves.

Figuring out vegetative defense strategies is more than just of passing interest to plant biologists. It’s also essential for ensuring the safety of world food supplies: Consider notorious plant predators such as late blight, which caused the famous Irish potato famine, or stem rust fungus, which first outwitted the immune system of wheat in Uganda in 1999 and has since spread to Kenya, Ethiopia, Sudan, and Iran, threatening food security in areas already facing geopolitical challenges.

UNWANTED GUEST
The fluorescent-dyed fungus Magnaporthe oryzae (green) invades rice cells (red).
Credit: Barbara Valent/Plant Cell © 2007
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UNWANTED GUEST
The fluorescent-dyed fungus Magnaporthe oryzae (green) invades rice cells (red).
Credit: Barbara Valent/Plant Cell © 2007

Pathogens that attack plants have a potpourri of break-and-enter techniques. Some saunter in or squeeze through open stomata, the pores plants use to exchange gases. The Pseudomonas syringae bacterium carries proteins that help freeze the water found on the surface of plant leaves, causing leaf cells to burst, thus creating a convenient entranceway into the plant. Some fungi have equipment called appressoria that use turgor pressure to push into a leaf cell like a hammer. Others have evolved enzymatic machinery that breaks down plant cell walls locally, says Paul Schulze-Lefert of the Max Planck Institute for Plant Breeding Research, in Cologne, Germany. “Just like a nutrient Hoover or a vampire, they suck up all the goodies but still keep the plant alive.”

Efforts to map out plants’ defense systems date back decades, but a major breakthrough occurred in 1995 when Pamela Ronald, now a plant geneticist at the University of California, Davis, went spelunking in the rice genome and pulled out a gene for the first receptor protein involved in plant immunity. The receptor, called Xa21, could recognize a broad variety of invading bacteria, and its activation limited the growth of the pathogens. “It took us about 15 years to figure out the receptor protein recognizes a short peptide that many bacteria use to communicate with each other,” Ronald says.

During this time, other researchers began to discover that plants contain a number of other receptors that recognize common features of invading microorganisms. These features include a component of bacterial flagella, the protein motors that many bacteria use to swim around, and chitin, a long-chain polymer of N-acetylglucosamine that is found in the cell walls of many fungi. The plant immunity community named the components of invading microorganisms that could activate these plant receptors MAMPs (microbe-associated molecular patterns) and PAMPs (pathogen-associated molecular patterns).

MAMP and PAMP receptors are the first line of defense for plants, Ronald says. “This plant innate immunity turns out to be very similar to the human innate immunity system, with similar protein receptors,” she explains. Once an invading microorganism is recognized by the innate immune system, a plant cell releases a molecular distress flare to warn other cells of the invasion. This flare is sometimes azelaic acid, which acts as a signal to plant cells to accumulate salicylic acid, an important component of the defensive response (Science, DOI: 10.1126/science.1170025).

With the innate immune system primed, plants are capable of suppressing the growth of many microorganisms. But how they manage to do so is mostly still a mystery.

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Unlike plants’ first line of defense, which simply recognizes the hallmarks of a potential invader and not its actual weapons, plants’ second line of defense takes aim at their microbial enemies’ artillery. When pathogens enter a plant cell, they don’t just put up their feet, relax, and call it a day. Instead they release dozens of different kinds of small molecules and peptides that effectively “bomb the plant cell,” Ronald says.

In dropping these bombs, pathogens typically aim to disable innate immunity, a plant’s first line of defense, says Jeff Dangl, a plant biologist at the University of North Carolina, Chapel Hill. “Pathogens can’t avoid being recognized,” he explains, “so they figured out a way to suppress the consequences of recognition via chemical warfare.”

For example, Sheng Yang He at Michigan State University and his colleagues figured out that some of these bombs are directed at shutting down a plant’s ability to export proteins—its so-called secretory output pathways (Science, DOI: 10.1126/science.1129523). “Part of a plant’s general defense response is to secrete a bunch of proteins that are probably bad for microbes. So smart microbes figure out ways to block that secretion,” Dangl explains.

Sometimes the pathogen’s artillery includes peptides that suppress the genesis, stability, and activity of microRNAs that plants produce during the initial innate immunity response (Science, DOI: 10.1126/science.1159505).

In other cases, the artillery contains chemicals that distract the plant from the imminent invasion by instructing the plant to invest its energy reserves in activities other than pathogen defense. For example, the fungus Gibberella fujikuroi injects the plant hormone gibberellin when it infects rice. Instead of launching a defense strategy, rice injected with the fungal hormone grows so fast that researchers refer to the ailment as “foolish seedling disease.” It turns out that gibberellins effectively suppress the rice’s defense hormone salicylic acid (Curr. Biol., DOI: 10.1016/j.cub.2008.03.060).

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Other pathogens such as P. syringae inject a chemical called coronatine that mimics the plant hormone jasmonic acid, thereby interfering with jasmonic acid signaling and causing the plant host to divert its immune response (Nature, DOI: 10.1038/nature09430). “Plant pathogens have figured out a way to fake out a plant and alter its gross regulatory responses away from defense,” Dangl says.

Faced with such cunning microbial adversaries and the sophisticated chemical weapons they possess, a plant’s second level of immunity is effectively a series of chemical countermeasures, leading to an intricate molecular arms race between plant and pathogen.

Evolving cellular machinery that recognizes every single type of bullet from every type of pathogen would be energy intensive. So plants have opted for a more efficient strategy, wherein they typically monitor cellular proteins that are “repeatedly targeted, over and over again, by many different strains of pathogens,” Dangl says. His team has discovered that multiple pathogens target a plant protein called RIN4 with different types of ammunition. RIN4 has an important role in a plant’s first line of attack, and different pathogens use different artillery to repeatedly phosphorylate RIN4, which reduces the plant’s ability to fight infection.

Because “RIN4 is hit over and over again,” resistant plants have evolved a guard protein that monitors that phosphorylation state of RIN4 instead of the artillery that pathogens use to phosphorylate it, Dangl says. When RIN4’s guard protein notices an abundance of phosphorylation, it quickly reboots the plant’s defenses by removing the phosphorylation. “A major topic over the next 10 years will be to figure out how that rebooting step works,” Dangl says.

The mechanism of this process is just one of the many mechanisms of plant immunity still left to be understood. Although plant biologists have identified major molecular players in the field of plant immunity, how those players cooperate as a team is still mostly unknown. “This field has been dominated by geneticists,” Dangl says. “We have a crying need for biochemists, computational chemists, and researchers that can build small molecules or do mass spectrometry and X-ray crystallography.”

Posttranslational modifications such as sulfation, glycosylation, and acetylation are just emerging as important players in the plant immune response, Ronald says, and constitute another area of research where chemical expertise is valuable.

Ronald also points out that many of the kinases involved in innate immunity are not the typical kinases that phosphorylate themselves or another protein. Instead, she says, “these kinases seem to function partly as phosphorylation-mediated scaffold proteins, as distinct from enzymes that mediate signaling through a ‘phosphorelay’ cascade.”

PRETTY MEAN
A dyed cross section of stem rust fungus (yellow/orange) invading a wheat plant (purple/green).
Credit: Leah Penn Boris
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PRETTY MEAN
A dyed cross section of stem rust fungus (yellow/orange) invading a wheat plant (purple/green).
Credit: Leah Penn Boris

Genomics studies are still revealing all sorts of new features of the battles between plant and pathogen. For example, comparative studies between the genomes of closely related microorganisms that differ only in their ability to infect a plant are revealing new virulence effectors just as similar genomic comparisons between plant species that are resistant or vulnerable to a particular pathogen are revealing new plant defense strategies. For example, in a recent Science paper, researchers led by Sophien Kamoun at the Sainsbury Laboratory, in Norwich, England, reported that genes involved in chromatin remodeling may have helped the late blight pathogen develop its nefarious infection tactics (DOI: 10.1126/science.1193070).

And just as researchers are trying to understand how humans coexist with trillions of microbes but still activate strong immune responses to select pathogens, plant biologists are also trying to understand how plants manage their microbial neighbors. “Our current understanding of the innate immune system in plants creates a paradox,” Schulze-Lefert says. “If MAMP and PAMP receptors detect highly conserved features of microbes and then initiate an immune response, how then can plants accommodate a beneficial microbial flora?”

“The past few years have witnessed paradigm-shifting advances in the field of plant-microbe interactions,” noted He in a Science commentary with Thomas Boller, a plant biologist at the University of Basel, in Switzerland (DOI: 10.1126/science.1171647). However, “our current understanding of plant-pathogen interactions is of a pioneering but preliminary nature.”

These and other researchers hope that a more sophisticated understanding of plant immunity will not only shed light on the defense strategies of the world’s ubiquitous green life forms but also enable the development of more sophisticated and targeted strategies for dealing with crop pests—making it no longer necessary to blanket agricultural land with broad-spectrum pesticides that kill many microorganisms, even the good ones, Schulze-Lefert says.

 
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