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On the Origins of Plant Immunity

The May Origins essay examined the origins of the immune system but focused exclusively on the microbial defenses animals use. Here, Claire Thomas examines what scientists are learning about the evolution of plant immunity—and whether there are any connections with animal immunity.

Most of us know the basics behind the “adaptive” immune system in mammals—thanks to school biology lessons about white blood cells that specifically attack and engulf pathogens or make antibodies that grab those microbes—but how do plants protect themselves?

At first glance, plant immunity is far simpler: Plants rely partly on their rigid cell walls to keep out microbes. They don’t have a circulatory system and therefore no roaming immune cells to track down bacteria and viruses. But they do have one fundamental thing in common with mammals: a basic “innate” immune system. In mammals, the white blood cells that make antibodies or specifically target microbes rise up only after this innate arm carries out the initial immune response to a pathogen, typically causing inflammation. Plants, on the other hand, can only use their innate responses to fend off pathogens.

But as scientists have compared plant and animal immunity, they’ve been struck by something surprising. “The current evidence and belief is that there is tremendous similarity between animal innate and plant immune systems,” says Dan Klessig, a plant pathologist at Cornell University. In fact, both systems use similar receptors to detect invading pathogens.

Which raises an intriguing issue: Did a primordial ancestor common to plants and animals evolve a basic innate immune system, which began to differ in the two lineages once they split (divergent evolution)? Or did plants and mammals evolve innate immunity independently but end up with similar mechanisms (convergent evolution)? That’s something that scientists have puzzled, and argued, over. “It’s an area where there’s more debate than data,” says plant geneticist Peter Tiffin of the University of Minnesota, Twin Cities.

Some of those limited data concern the molecular details of how plant and animal cells recognize a pathogen and transmit that signal to prompt defensive actions. At the center of the debate over convergent or divergent evolution are the pattern recognition receptors (PRRs), the host proteins that detect molecular features of invading pathogens, such as their DNA or bits of proteins, and kick-start the innate immune response in both groups. If one looks at PRRs in plants and animals, the molecules all share a key structural element, a section rich in leucine amino acids that is used by the receptor to bind and recognize bits of a pathogen.

A diagram depicting a mammalian cell and a plant cellP. Huey/Adapted from Nature

Beyond that leucine-rich repeat (LRR) region, the PRRs of plants and animals often share other structural components that help the receptors transmit a signal once activated. The Toll-interleukin 1 receptor (TIR) domain, a key signaling component of microbial receptors that sit on the surface of animal cells, is also part of microbial receptors found within the cytoplasm of plant cells. And both plant and animal PRRs in the cytoplasm have similar nucleotide-binding sites (NBS), portions of the protein that bind to the energy molecule ATP to help activate the receptor. This presumably leads to reactions that regulate genes involved in the innate immune response. Overall, it’s the PRRs within the cytoplasm (called nucleotide-binding domain leucine-rich repeat containing, or NLR, proteins) versus the ones that span the cell membrane that look the most similar between plants and animals (see diagram, P. Huey/Adapted from Nature). “The structural similarities are just compelling and striking,” says plant-microbe interaction expert Paul Schulze-Lefert of the Max Planck Institute of Plant Breeding Research in Cologne, Germany. “Why did [plants and animals] choose the same building blocks to build surface receptors and intracellular sensors?” he muses.

Still, Schulze-Lefert and others believe there may be a very trivial explanation behind this. There are only a limited number of proteins and chemicals that can be used to build receptors and biochemical pathways, Schulze-Lefert says. Or as geneticist Fred Ausubel of the Harvard Medical School in Boston put it in a 2005 review on the evolution of innate immunity: “There are inherent constraints on how an innate immune system can be constructed.”

In addition, although similar proteins are used, they don’t necessarily function in the same way. Both plants and mammals have analogous cell-membrane receptors that detect the bacterial protein flagellin – FLS2 (in Arabidopsisplants) and TLR5 (humans). But the two receptors detect different regions of the flagellin protein. “In my view, this is strong evidence for convergent evolution,” Schulze-Lefert says.

Ausubel also points out that if there were a common unicellular ancestor in which innate immunity evolved, these molecular components of the PRRs should be present not only in plants and animals but also in green algae, fungi, and choanoflagellates that share the same common ancestor (see diagram below). “But fungi and choanoflagellates don’t have [NLR] proteins,” he says, revealing a potential gap in evolutionary inheritance. However, he stresses that the fungi conundrum “doesn’t prove the case”—these proteins could simply have been lost in evolution.

If a common ancestor of plants and animal had an innate immune system, this phylogeny of life indicates that several other branches, such as fungi, could have remnants of it too.University of California Museum of Paleontology

If a common ancestor of plants and animal had an innate immune system, this phylogeny of life indicates that several other branches, such as fungi, could have remnants of it too.

Immunologist and geneticist Bruce Beutler, on the other hand, believes the evidence points to a common origin of a PRR that has since been copied, modified, and adapted. The use of similar protein motifs, such as TIRs and LRRs, in plant and animal defenses is “pretty suggestive that the ancestral protein had a defensive function,” says Beutler. It “would be quite a coincidence” for both plant and animal innate systems to have evolved independently, he says.

“We can’t know for sure,” but the occurrence of these protein motifs in both plants and mammals is “strong evidence [of divergence], and it will grow stronger in time,” predicts Beutler.

All sides agree that the argument is far from clear-cut, and a lack of data is preventing scientists from reaching a consensus on the evolution of innate immunity. In an attempt to fill some of the gaps, Ausubel is currently investigating the phylogeny, or evolutionary relatedness, of the intracellular PRR proteins. “There’s been a lot of speculation based on relatively little data,” he says. A paper from his group, which is due out later this year, will show that those similar-looking microbial receptors in plants and animals are actually derived from separate evolutionary ancestors, says Ausubel. It will be interesting to see what both camps make of the findings.