No place to run

Abstract

Science & Society25 March 2018free access No place to run Plants have evolved a dazzling array of chemical defences and regulatory networks that matches the mammalian immune system for complexity Philip Hunter Freelance journalist [email protected] London, UK Search for more papers by this author Philip Hunter Freelance journalist [email protected] London, UK Search for more papers by this author Author Information Philip Hunter1 1London, UK EMBO Rep (2018)19:e46020https://doi.org/10.15252/embr.201846020 PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info Plants never had it easy. When their ancestors colonized the land about 460 M years ago during the Ordovician period, they were immediately followed by crustaceans—which eventually developed into insects—that found plants a ready source of food. Ever since plants have been at the bottom of the food chain for pathogens and predators from viruses to mammalian herbivores. Unlike animals, plants cannot run away, having given up motility to maximize their surface exposed to sunlight. In lieu, they became masters in chemical warfare and communication to recognize and fend off pathogens and herbivores. Their “claws and teeth” are a dazzling arsenal of chemicals, metabolic and regulatory pathways, producing sensing and communication molecules that attract increasing interest from chemists and biologists for their potential use in medicine and agriculture. Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. Among these molecules are many spices, including the pungent piperine and capsaicin from peppers, or the glucosinolates from mustard and horseradish, and the bitter polyphenols, flavonoids or terpenes from red grapes, coffee beans, tea or cabbage. Humans have long come to appreciate these tastes—that originally evolved as a warning signal to herbivores—for centuries, spices were the most valuable commodity in global trade. Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. The alkaloid taxol from the bark of the Pacific yew is a potent chemotherapeutic drug for cancer treatment; artemisinin, isolated from the plant Artemisia annua, or sweet wormwood, has long been employed in Chinese herbal medicine and been refined into a treatment for malaria. The metabolic pathways of plant compounds with medicinal value are therefore an active field of research with the objective of engineering these into E. coli or yeast for manufacturing the drugs at scale by fermentation. Knowledge of the defensive pathways can also be exploited to improve the resilience of crop varieties. Many food crops have been heavily selected for yield and lost defensive capabilities and stress tolerance, thus leading to yield losses from both biotic and abiotic factors. These losses are notoriously hard to measure with disagreement over whether to count yield, revenues or qualitative factors and vary greatly between crops and locations. The best rough guide comes from a survey, which estimated total annual losses due to all factors in the range of 26–29% for soybean, wheat and cotton, 31% for maize, 37% for rice and as high as 40% for potatoes (http://www.davidmoore.org.uk/21st_Century_Guidebook_to_Fungi_PLATINUM/Ch14_01.htm). Of these losses, 18% on average are attributable to animal pests, 16% to microbial disease with fungi accounting for around 75% of those and finally 34% due to weeds. Hormone-controlled networks One fundamental insight into plant defences is that these compounds do not operate in isolation, but as large networks underpinned by phytohormone signalling. These networks interact with pests, pathogens and the wider environment in a complex way that depends not just on the plant itself but also on these confounding factors. Phytohormones, unlike their animal counterparts, are produced by every cell rather than specialized glands and tend to occur in lower concentrations. Like their animal equivalents, they regulate vital metabolic and developmental processes, including flowering, leaf and fruit development, and defence. These roles interact so that a plant's immune or defensive status varies with the season as well as on a day-to-day basis. It is this interaction that lies at the root of plants’ flexibility in responding to a wide range of threats. One fundamental insight into plant defences is that these compounds do not operate in isolation, but as large networks underpinned by phytohormone signalling. Until around 5 years ago, it was thought that two phytohormone pathways dominated plant defences: the jasmonic acid (or jasmonate) and salicylic acid pathways. The jasmonic acid pathway plays a crucial role in defending against insect herbivores and necrotrophic pathogens, primarily fungi that destroy plant tissue first and feed on the resulting dead cells 1. This paper presented evidence of a causal link between wounding by insect herbivores, the formation of jasmonic acid derivatives and induction of genes for proteinase inhibitors that deter insect feeding by making the plant material less digestible. Since, it has become clear that the jasmonic acid pathway plays a broad role against a range of biotic and abiotic insults and stress factors. A recent study showed that, under controlled conditions, it is possible to induce cannibalism among caterpillar predators (Spodoptera exigua) by triggering the jasmonic acid pathway. The salicylic acid pathway is invoked in defence against biotrophic pathogens that obtain nutrients from living cells, including viruses, bacteria and some microfungi 2. These are combated by the plant's innate immune system, which is activated by pathogen-associated molecular patterns (PAMPs) on the pathogen's surface. PAMPs are received by plant pattern recognition receptors (PRRs), which then pass the messages on to various signalling hormones, of which salicylic acid is usually the most important. The evolution of these and other phytohormone pathways began around the time plants colonized land 500 million years ago. Since, hormonal pathways and their crosstalk settled around conserved hubs that are common to most plants. “Although plant hormone signalling pathways are very well conserved in plants, it appears that crosstalk between pathways is different in different species”, Tsuda commented. “So by learning about evolution of hormone crosstalk, we might be able to develop a sustainable strategy to improve agriculture”. One recently discovered aspect of these two pathways is that they interact negatively with each other. “The jasmonic acid pathway plants activate against herbivores often seems to work against the salicylic acid pathway against microbes”, explained John Orrock, who specializes in plant defence signalling information at the Department of Integrative Biology, University of Wisconsin, USA. “So it is hard for plants to deal with both at once”. This antagonism has been exploited by some necrotrophic pathogens, including the fungus Botrytis cinereal, a scourge of grape vines, and Alternaria solani in tomatoes 3. This study found that these fungal necrotrophs manipulate the salicylic acid signalling pathway to boost its production, which then suppresses two jasmonic acid-dependent protease genes that make the plant less digestible. However, such antagonism can itself provide a target for human intervention to confer better resistance against pathogens and insect herbivores. “We have written a review about engineering hormone crosstalk to potentially improve crop production, 4” said Kenichi Tsuda, Group Leader of the Department of Plant Microbe Interactions at the Max Planck Institute for Plant Breeding Research in Cologne, Germany. “[O]ne promising way is to disconnect links between hormone signalling pathways. For instance, growth and defence suppress each other, known as growth-defence trade-off”. As Tsuda noted, this enables plants to compromise between growth and defence, or between different kinds of defence. But human engineering coupled with help on the ground, such as fertilizers, can uncouple this connection to the effect that plants defend themselves without sacrificing growth—or such is the theory. “Considering people's objections to GMOs, engineering is not realistic in the near future”, Tsuda commented. “We would need to investigate multiple related species to extract wanted traits and breed traditionally. Then if CRISPR technology is accepted by society in future, it would become much easier because genetic changes at the interlink between pathways can be made technically”. Manipulating hormonal crosstalk Meanwhile, insight into the mechanisms of plant defence hold promise of direct manipulation without engineering hormonal crosstalk. In the case of insect herbivores, one possibility lies in exploiting the tendency of these predators to fall back on cannibalism when the plants on which they are feeding are either consumed, lose nutritional value or otherwise become harder to eat. A recent study showed that, under controlled conditions, it is possible to induce cannibalism among caterpillar predators (Spodoptera exigua) by triggering the jasmonic acid pathway 5. This stimulates production of various chemicals, including phenolic molecules that reduce palatability, such as flavonoids, isoflavonoids, anthocyanins and lignins. In the study, tomato plants were sprayed with four different preparations of the volatile methyl jasmonate. Plants sprayed with jasmonate caused herbivores to start consuming each other; this happened earlier, the higher the jasmonate concentration. The control plants were almost completely defoliated while those given the highest jasmonate dose ended up with the greatest biomass and least damage. The ability to signal an attack quickly to other parts of the plant outweighs the disadvantages of helping nearby competitors… According to lead author Orrock, this induction of cannibalism benefits plants both by diverting the caterpillars to feed on each other and by reducing their numbers. He also suggested that the dose level might be crucial to induce cannibalism before much damage had been done. “The worst-case scenario is that caterpillars only eat each other only after the entire plant has been consumed”, Orrock added. He also argued that induction of cannibalism could play a much bigger role in natural plant defence than has been appreciated: “The thing to realize is that cannibalism among insects is quite widespread, even among those typically not thought to be, such as those that eat plants. After all, if there's anything that might meet your nutritional requirements, it's eating organisms exactly like you”. This ability to trigger cannibalism has potential for agriculture but would require bigger field studies in more natural conditions. “We need to understand the interplay between all these factors, which is a whole new game”, Orrock commented. A delicate balance Such studies have though increased knowledge of how plants handle the balance between defence and growth: some use a “constitutive defence” to be ready for attack by insect herbivores in particular. Others rely more on induced defences that are turned on only in response to signals, so they can focus on growth and reproduction when there is little or no threat of consumption. “The key lies in the reliability of the cue”, Orrock explained. If the plant receives reliable cues and has time to react before it suffers serious damage, it can concentrate on growing until signals arrive. If the signals are unreliable or inconsistent, the plant cannot afford to rely on them and will more likely have some permanent defences. Signals can be generated in direct response to attack or indirectly when predators are in the vicinity. They can be transmitted within the plant through its vascular system or via air such as methyl jasmonate, which has the advantage of being faster, but more susceptible to environmental conditions. Apart from the advantage of speed, airborne signals are almost the only form of communication for plants in environments such as arid regions that have limited capacity for internal transmission of information because of limited water. Airborne signals are conveyed by a variety of volatile organic compounds (VOCs), including phenolics and tannins. Methyl jasmonate emitted by sagebrush (Artemisia tridentata) was the first compound shown to render plants resistant to herbivores even when no direct contact with the predator had yet occurred 6. Moreover, VOCs are also detected by neighbouring plants and by other parts of the emitting plant in response to attack. This raises the obvious question of the evolutionary basis of airborne signalling, given that it increases the fitness of neighbouring plants, even different species. By making competing nearby plants fitter, the emitter would by definition be at a competitive disadvantage against its neighbours. This debate has not been settled, given that neighbouring plants do benefit from VOCs emitted nearby 6, but there is mounting consensus that it was driven by selection for intra-plant communication. “I and several others argue that the “true” function of resistance-induction by volatiles is within-plant signalling, and that the responses in neighbouring plants result from eavesdropping rather than true communication”, said Martín Heil, head of the plant ecology laboratory at CINVESTAV-Irapuato in Mexico. The ability to signal an attack quickly to other parts of the plant outweighs the disadvantages of helping nearby competitors, according to this argument. Furthermore, there may be a general advantage for a whole plant ecosystem in cooperating. Heil agreed that in evolution, it is difficult to distinguish between primary and secondary roles of any property such as signalling: the main point is that the emitter of a signal must gain some overall advantage even if there are some negative aspects. Recruiting fungi for defence The bigger question, which is still open according to Heil, is how plants perceive these VOCs in the first place and how specific the cues are. “We still don't know the nose of plants”, he said. “Chemically diverse volatiles often trigger similar responses and nobody can explain how, for example, C6 alcohols, esters and terpenes, can trigger the same responses”. The plant does have a nose, albeit distributed over its surface, but it is not clear yet which predators and pathogens generate cues that stimulate it. “The vast majority of studies so far refer to defence against insect herbivores”, Heil said. “I am not aware of a report on viruses, and to the best of my knowledge, my own papers are the only reports on volatile-mediated resistance to bacteria and fungi”. The overall role of fungi in plant defence has also attracted interest, since these are the biggest source of disease in plants, but can also protect the plant against other predators and pathogens The work on fungi showed that volatiles can have a dual function with anti-fungal activity and as signals that switch on other resistance genes in the plant. It also relates to other work highlighting how volatiles elicited by an insect herbivore can induce or increase generation of protective fungi that attack such predators. One study showed that volatiles induced by aphid attacks promoted generation of the fungi Lecanicillium lecanii, which infects these insects 7. The overall role of fungi in plant defence has also attracted interest, since these are the biggest source of disease in plants, but can also protect the plant against other predators and pathogens. Endophytic fungi—parasites that derive nutrients from their host without causing damage—can protect against both disease and herbivores, as well as other stress factors such as drought, heat, salt and metals. Recent work has further elucidated their symbiotic contribution. One study found that in addition to producing protective alkaloids, endophytic fungi enhance plant immunity against chewing insects by promoting various endogenous defences mediated by the jasmonic acid pathway 8. This too offers potential for enhancing defences against herbivory. Another important aspect of plant defences that emerged earlier from research on the jasmonic acid pathway is the phenomenon of “stress memory”, which is the basis of systemic acquired resistance (SAR) in plants. It confers resistance by triggering a systemic response after localized exposure to a pathogen or stress factor. However, the priming can also confer immunity against future attack from given pathogens or herbivore predators and thus operates similar to adaptive immunity in animals. In silico defences Plants can also employ minerals to bolster their defences; for instance, silica can render plant material harder to consume. “Silicon is used by plants to defend against a range of plant predators, from fungal pathogens and invertebrates to mammals and possibly even dinosaurs”, commented Julia Cooke, Lecturer in Ecology at the Open University in the UK. “Silicon can help protect against invertebrates, including those that bore in stems and roots, munch leaves, and feed on the phloem and xylem. […] There is good evidence that silicon makes plants less attractive to mammalian herbivores, reducing palatability, and higher silicon content also decreases how much nutrient they can extract from plants by reducing digestibility. Much of the recent work on mammals and plant silicon defence has centred around voles, but there is also an impressive body of research looking at the way silicon accumulation in grasses can be induced in response to large mammal grazing”. Silica deters herbivory by wearing down the animal's teeth or by impairing digestion. But again, it comes at a cost, which is why some plants employ silica much more than others. “Silica is quite dense and heavy, so plants that accumulate lots of silicon in their leaves might need to invest more heavily in stem strength”, Cooke explained. “Another limitation might be that silicon does not form many types of compounds—mainly silica. Carbon, in comparison, can be used to make all sorts of proteins with different functions, so some plants may have evolved not to accumulate much silicon because of its lack of versatility, instead finding other defence mechanisms better increase fitness”. Nonetheless, silicon defences are quite common, presumably because they are inducible and act against a wide range of predators. More notably, silicon accumulation seems again to be stimulated by symbiotic fungi. A recent study by Adam Frew and colleagues at Charles Stuart University Wagga Wagga in Australia found that the presence of arbuscular mycorrhizal fungi, which have relationships with around 80% of vascular plants, can increase silicon concentrations and thereby enhance plant defences against herbivory 9. It is thus yet another example of how plants are able to integrate and manipulate their biotic and abiotic environments in a network of interactions that matches the mammalian immune system in complexity. Growing understanding of how all these factors fit together and interact through signalling pathways remains a major challenge for plant research, but such research could yield enormous benefits for agriculture, medicine and sustainable development.