Caterpillars use bacteria to produce green islands in yellowing leaves

By Ed Yong | March 30, 2010 7:00 pm

Green_islandIn autumn, as green hues give way to yellows and oranges, some leaves develop mysterious green islands, where life apparently holds fast against the usual seasonal decay. These defiant patches still continue the business of photosynthesis long after the rest of the leaf has withered. They aren’t the tree’s doing. They are the work of tiny larval insects that live inside it – leaf-miners.

The larvae were laid within the leaf’s delicate layers by their mother. They depend on it for shelter and sustenance, and they can’t move away. If their home dies, they die, so they have a vested interest in keeping at least part of the leaf alive. These are the miniature landscape architects that create the green islands, and they don’t do it alone – to manipulate the plant, they wield bacteria.

Wilfried Kaiser and scientists from Rabelais University discovered this partnership after realising that some bacteria and fungi can also cause green islands. He reasoned that microbes might be helping insects to achieve the same ends. So he searched for them in one particular species, a tiny moth called the spotted tentiform leaf-miner, Phyllonorycter blancardella. Its larva makes its home in the leaves of apple trees.

Kaiser found that the leaf-miners are host to just one detectable type of bacteria – Wolbachia. That’s hardly surprising. Wolbachia infects around 60% of the world’s insect species, making it a strong candidate for the title of world’s most successful parasite. Without exception, every leaf-miner that Kaiser tested, from all over the Loire Valley, carried Wolbachia in their tissues.

The bacteria were the true agents behind the green islands. When Kaiser cured the leaf-miners of their infections using antibiotics, they seemed perfectly healthy. But they completely lost the ability to stem the yellowing of leaves. As a result, 85% perished before adulthood; for comparion, the typical mortality rate of Wolbachia-carrying larvae is just 10%. Worst of all, since Wolbachia is passed down from mother to offspring, later generations also suffered the same lack of beneficial bacteria, the same inability to produce green islands and the same high odds of an early death.

Leaf-minersThe bacteria manipulate the leaves using their own signalling chemicals – a group of plant hormones called cytokinins. These substances perform many tasks in a leaf: they maintain the supply of chlorophyll; they prevent the leaf from dying; and they control the flow and storage of nutrients. They’re the barrier that stands between a living leaf and a rotting one. Stick cut plants in cytokinin solution and they’ll stay green for longer. What better tool for a bacterium or an insect looking to prolong the life of its leafy home?

Inside a typical mine, levels of cytokinins are much higher than usual. But when Kaiser cured the leaf-miners of Wolbachia, he found that the levels of cytokinins in the mine plummeted to levels typically seen in yellow leaves.  Without these hormones, the insects failed to protect their homes. And if Kaiser injected cytokinins into leaves directly, he could create green islands on his own, without the need for either Wolbachia or a leaf-miner.

We know that the bacteria are necessary for the cytokinin flood that maintains the mine, but the exact source of these chemicals is unclear. It’s possible that the bacteria secrete them directly, or allow the leaf-miner to do so. Indeed, Wolbachia has a gene that’s important for the creation of cytokinins, and a paper published four decades ago found large amounts of these hormones in the salivary glands of a leaf-miner. The other alternative is that the bacteria encourage the plant to over-produce its own hormones. Of course, all of these possibilities could be working together.

Of course, many insects have their own beneficial resident bacteria, or symbionts. These tenants provide them with valuable nutrients that they can’t make themselves, and they can even offer protection against enemies and environmental challenges.  But this is the only known example of an insect using a bacterial symbiont to directly manipulate a plant, and it seems to be a successful strategy.

By all accounts, leaf-mining is an evolutionary success story, and hundreds of species have adopted this lifestyle. Their partnership with bacteria might be the secret of their success but Kaiser will only know that for sure once he works out how widespread the use of bacteria is, and what these microbes actually do to the plant.

Reference: Kaiser, W., Huguet, E., Casas, J., Commin, C., & Giron, D. (2010). Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2010.0214

Images: by Kaiser

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Comments (11)

  1. Christina

    Fascinating! I had no idea that Wolbachia could have a symbiotic relationship with its host – I was under the impression that they were solely parasitic

  2. Brian Too

    Sorry, these links don’t work. Or more accurately, they work but there’s no content at the destination. The expected Wolbachia article just ain’t there.

  3. Megan

    If you enter “an-entire-bacterial-genome-discovered-inside-that-of-a-fruit-fly” into google, you can get the entry that way; it’s the first link.

    Or, you can just go to the old site: http://notexactlyrocketscience.wordpress.com/2007/08/30/an-entire-bacterial-genome-discovered-inside-that-of-a-fruit-fly/

  4. Nathan Myers

    Funny, I found it at http://scienceblogs.com/notrocketscience/2009/07/an_entire_bacterial_genome_discovered_inside_that_of_a_fruit.php .

    I notice that since 2007, the fraction of insects parasitized by W. has increased from 20% to 60%. That’s fast work!

  5. Ok I’ve fixed all the links. They should all work now.

  6. Art

    Does Wolbachia infest 20% of insect species, like the link says, or 60%, as stated in this article?

  7. Right, I’ve found the reason behind the differing stats.

    The 20% figure came from this story based on this paper, which said “Wolbachia… infects a wide range of arthropods, including at least 20% of insect species”. For that statement, it cites this paper but if you actually look at it, it doesn’t mention a 20% stat anywhere! It says that “at least 16% of neotropic insects are infected with W. pipientis”, which may have become rounded up, but neotropical insects aren’t all insect species.

    Meanwhile, the 60% figure comes from this story based on this paper, which says “Wolbachia… are estimated to infect more than 60% of all insect species.” For that stat, it cites this paper, which says:

    “Estimates suggest that at least 20% of all insect species are infected with Wolbachia these estimates result from several Wolbachia screenings in which numerous species were tested for infection; however, tests were mostly performed on only one to two individuals per species. The actual percent of species infected will depend on the distribution of infection frequencies among species. We present a meta-analysis that estimates percentage of infected species based on data on the distribution of infection levels among species. We used a beta-binomial model that describes the distribution of infection frequencies of Wolbachia, shedding light on the overall infection rate as well as on the infection frequency within species. Our main findings are that (1) the proportion of Wolbachia-infected species is estimated to be 66%.”

  8. Lizzy Wilbanks

    This stuff is fascinating. Thanks for bringing this great new study to my attention! Michael Turelli’s lab at UC Davis has been doing really interesting research on the wolbachia-mutualist question for some time: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1852586/

  9. May I get a copy on line of your recent paper on Plant green-island …publshed into PRS B April 07 2010?
    Thanks.

  10. MGourley

    I know this post is a little late, but as a Wolbachia researcher, I wanted to address the issue of contradicting estimations of Wolbachia infection frequencies in arthropod populations. The comment from Ed Young highlighted how inconsistent published reports of Wolb infection rate/status can be.

    So here’s the problem: Most animals on the planet are arthropods. Think about it, every insect and bug, every crustacean (ie: lobsters and crabs)- they are all arthropods and there are TONS of them! This means that it is nearly impossible to survey all arthropds to determine their Wolbachia-infection status. We can’t even get close to looking at “most” of them.
    Even when research groups DO look for Wolbachia, its hard to maintain one central, current list of who has Wolb and who doesn’t.
    The majority of arthropods that HAVE been surveyed do seems contain Wolbachia, which makes some researchers think that about 90% of arthropods contain Wolb. But other, more conservative and hesitant scientists don’t think enough arthropods have been surveyed to justify such a big percent estimation, and claim 20% Wolb infection.

    As a result, many researchers will publish 20-90% in efforts to appease all of the authors and reviewers involved in getting a publication into print.

    TAKE HOME POINT: No one knows how many arthropods have Wolbachia, but since arthropods are the most abundant animals on the planet, and since many arthropods seem to be infected with Wolbachia, that makes Wolbachia a bacteria of pandemic proportions!

    Great blog! Thanks for spreading the word about Wolbachia!

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