A new study led by the University of Oxford has used a modelling approach to show that it is unlikely that plants would evolve to warn other plants of impending attack. Instead of using their communication networks to transmit warning signals, the findings suggest it is more likely that plants 'eavesdrop' on their neighbours. The study has been published this week in the journal Proceedings of the National Academy of Sciences (PNAS).
Our results indicate that it is more likely that plants will behave deceptively toward their neighbours, rather than altruistically...Plants can gain a benefit from dishonest signalling because it harms their local competitors, by tricking them into investing in costly herbivore defence mechanisms.
Lead author Dr Thomas Scott , (Department of Biology, University of Oxford)
Land plants can be connected to a complex, underground fungal network known popularly as 'the wood wide web.' Networks emerge because mycorrhizal fungi form symbiotic partnerships with plant roots, through which the plants receive nutrients and the fungi receive carbon. It has been demonstrated that plant resources and information can be transmitted through the mycorrhizal network, and be used by other individuals.
Previous studies have found that, if a plant is attacked by a herbivore or pathogen, this often leads to other plants connected to the same fungal network upregulating their defence mechanisms. However, it has not been clear whether plants being attacked by herbivores actively signal through this network, to warn others to activate their defences.
Active signalling between plants appears to contradict evolutionary theory, which suggests that this kind of behaviour would only be favoured when it provides a benefit to both the sender and the receiver of the signal. This presented a conundrum for researchers - why should a plant being attacked send signals to warn its neighbours?
To investigate this, a team of researchers led by the University of Oxford in collaboration with Vrije Universiteit Amsterdam, used mathematical models to investigate different hypothetical conditions. They found that it is extremely hard to find situations where plants would be evolutionarily selected to warn their fellows of impending attack. The likely reason for this is that plants compete with neighbours for resources such as sunlight and nutrients, and so do not benefit from helping neighbouring competitors. In fact, the results indicated that plants can even be favoured to signal dishonestly to harm their neighbours.
Lead author Dr Thomas Scott , (Department of Biology, University of Oxford), who carried out the mathematical analyses, said: 'Our results indicate that it is more likely that plants will behave deceptively toward their neighbours, rather than altruistically. For instance, plants may signal that a herbivore attack is occurring, even when no herbivore is present. Plants can gain a benefit from dishonest signalling because it harms their local competitors, by tricking them into investing in costly herbivore defence mechanisms.'
The new findings challenge the idea that plants behave altruistically and suggests that we need to consider alternative hypotheses.
The mathematical models found that there are two viable alternatives that can explain why neighbouring plants upregulate their defence mechanisms when one is attacked. Potentially, plants cannot suppress sending out a cue that they are being attacked - even though they would not like this information being passed to neighbours, they cannot prevent it. Just like how humans cannot help blushing when they are embarrassed.
Mycorrhizal mushroom in Terra del Fuego. Credit: Mateo Barrenengoa.Another possibility is that fungi monitor their host plants, detect when they are attacked, and then warn other plants in their network. This intriguing possibility makes evolutionary sense because fungi could gain a benefit from helping to protect all the plants they are trading resources with.
'Maybe it is the fungal networks themselves that are sending the warning signals' added Dr Scott. 'Mycorrhizal fungi rely on the plants on their network for carbohydrates, so it's important to keep these plants in good condition. Perhaps the fungi are listening in on their plant partners, detecting when one has been attacked, and warning the others to prepare themselves.'
Co-author Professor Toby Kiers (Vrije Universiteit, Amsterdam) and Executive Director of Society for the Protection of Underground Networks ( SPUN ) added: 'There is no dispute that information is transferred. Organisms are constantly detecting and processing information about their environment. The question is whether plants are actively sending signals to warn each other. Maybe just like gossiping neighbours, one plant is simply eavesdropping on the another.'
The paper 'The evolution of signalling and monitoring in plant-fungal networks' has been published in Proceedings of the National Academy of Sciences (PNAS).
