Ten Papers that Shook My World – Haukioja & Niemelä (1976) – the plant “immune response”

To me this is a landmark paper, both personally and for ecology in general.   I first came across it in the second year of my PhD at the University of East Anglia (1978) and given where it was published, would probably never have seen it if my supervisor, Tony Dixon, hadn’t had a collaborative link with Erkki Haukioja of Turku University (Finland).

That individual plants of the same species are more or less susceptible (constitutive or innate resistance) to pests and diseases has been known for a very long time (e.g. Painter, 1958; Beck, 1965) and has been exploited by plant breeders as part of many pest management programmes.  Despite the stunning footage of the questing bramble in David Attenborough’s classic documentary The Private Life of Plants, plants are often thought of as passive organisms.  The idea that plants might actually respond directly and quickly to insect attack was more in the realms of science fiction than science fact, but this all changed in the 1970s. In 1972 a short paper in Science (Green & Ryan, 1972) suggested that plants might not be as passive as previously thought. Green & Ryan working in the laboratory with the Colorado Potato Beetle, Leptinotarsus decemlineata, showed that when tomato leaves were damaged by beetle feeding the levels of a proteinase inhibitor were raised not just in the wounded leaves but in nearby leaves as well. As proteinase inhibitors were well-known to be part of the plant defence system, they hypothesised that this was a direct response of the plant to repel attack by pests and that it might be a useful tool in developing new pest management approaches. So what does this have to do with two Finnish entomologists?

Erkki Haukioja and his long-term collaborator, Pekka Niemelä were working on an important lepidopteran defoliator of birch, in the far north of Finland, at the Kevo Subarctic Research Station.Kevo

http://www.eu-interact.org/field-sites/finland-4/kevo/

The defoliator that they were working on was the autumnal moth, now Epirrita autumnata, but then Oporinia autumnata.

Epirrita

http://ukmoths.org.uk/show.php?bf=1797

The autumnal moth, as with many tree-feeding Lepidoptera, has a 7-10 year population cycle (Ruohmäki et al., 2000).

Population cycles

Natural enemies are often cited as the causes of these cycles (Turchin et al., 1999) although other factors such as weather (Myers, 1998) or even sunspot activity (Ruohmäki et al., 2000)

Sunspot

have also been suggested. It had also been suggested that the marked population cycles of the larch bud moth, Zeiraphere diniana were caused by changes in the susceptibility of their host trees after defoliation (Benz, 1974). In 1975, Haukioja and his colleague Hakala, attempting to explain the cyclical nature of the E. autumnata population cycles wondered if they were being driven by the insects themselves causing changes in the levels of chemical defence in the trees. To test this Erkki and Pekka did two neat field experiments, remember Green & Ryan’s work was laboratory based and did not test the effects seen on the insects. They first fed Epirrita larvae on foliage from previously defoliated and undefoliated birch trees and found that the pupae that developed from those larvae fed on previously defoliated trees were lighter than those that had fed on previously undefoliated trees (Hauikioja & Niemelä, 1976). At the same time they also did an experiment where they damaged leaves but then rather than feeding the larvae on those leaves, fed them on nearby adjacent undamaged leaves and compared them with larvae feeding on leaves from trees where no damage had occurred. Those larvae feeding on undamaged leaves adjacent to damaged leaves grew significantly more slowly than those feeding on leaves that came from totally undamaged trees (Haukioja & Niemelä, 1977). So pretty convincing evidence that the trees were responding directly to insect damage and altering their chemistry to become more resistant, i.e. an induced defence and not a constitutive one.

Their results had a major impact on the field. The great and the good from around the world found it a fascinating subject area and a plethora of papers investigating the effects of insect feeding on induced defences in birch and willow trees soon followed (e.g. Fowler & Lawton, 1984a; Rhoades, 1985; Hartley & Lawton, 1987) and not forgetting the original researchers (e.g. Haukioja & Hahnimäki, 1984). I, with the aid of colleagues, also added my ‘two pennorth’ (I did say the idea shook my world) by extending the concept to conifers (Leather et al., 1987; Trewhella et al., 1997). The terms rapid induced resistance and delayed induced resistance soon entered the language, the first to describe those changes that occurred within minutes of feeding damage and the second, those that did not take effect until the following year (Haukioja & Hahnmäki, 1984; Ruohmäki et al., 1992) Such was the interest generated by the topic that by 1989 there were enough studies for a major review to be published (Karban & Myers, 1989).

Controversy reared its ugly head early on when Doug Rhoades suggested that not only did plants resist insect attack actively but that they could talk to each other and warn their neighbours that the ‘bad guys’ were in the neighbourhood (Rhoades, 1983, 1985). This sparked a brief but lively debate (e.g. Fowler & Lawton, 1984b, 1985). Ironically it is now taken as axiomatic that plants talk to each other using a range of chemical signals (van Hulten et al., 2006; Heil & Ton, 2008) as well as informing the natural enemies of the pests that a suitable food source is available (e.g. Edwards & Wratten, 1983; Amo et al., 2013; Michereff et al., 2013).

Ton cartoon

A great cartoon from Jurriaan Ton at Sheffield University. https://www.shef.ac.uk/aps/staff-and-students/acadstaff/ton-jurriaan

We now have a greatly increased understanding of the various metabolic pathways that induce these defences against different insect pests (e.g. Smith & Boyko, 2007) and can, by genetically manipulating levels of compounds such as jasmonic and salicyclic acids or even applying them directly to plants affect herbivorous insect communities and their natural enemies thus improving crop protection (e.g. Thaler, 1999; Cao et al., 2014; Mäntyllä, 2014). No wonder this was an idea that shook my world, and yours.

 

Post script

The study of induced plant defences or resistance is now dominated by molecular biologists and current practice is to use the term priming and not induced defence. The increased understanding that this new generation has brought to the field is undeniable but I always feel it is a great shame that they seem to have forgotten those early pioneers in the field.

 

References

Amo, L., Jansen, J.J., Van Dam, N.M., Dicke, M., & Visser, M.E. (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecology Letters, 16: 1348-1355.

Baldwin, I.T. & Schultz, J.C. (1983) Rapid changes in tree leaf chemistry, induced by damage: evidence for communication between plants. Science, 221, 277-279.

Beck, S.D. (1965) Resistance of plants to insects. Annual Review of Entomology, 10, 207-232.

Benz, G. (1974). Negative Ruckkoppelung durch Raum-und Nahrungskonkurrenz sowie zyklische Veranderung. Zeitschrift für Angewandte Enomologie, 76: 196-228.

Cao, H.H., Wang, S.H., & Liu, T.X. (2014) Jasomante- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Science, 21, 47-55.

Edwards, P.J. & Wratten, S.D. (1983) Wound induced defences in plants and their consequences for patterns of insect grazing. Oecologia, 59: 88-93.

Fowler, S.V. & Lawton, J.H. (1984a) Foliage preferences of birch herbivores: a field manipulation experiment. Oikos, 42: 239-248.

Fowler, S.V. & Lawton, J.H. (1984b) Trees don’t talk : do they even murmur? Antenna, 8: 69-71.

Fowler, S.V. & Lawton, J.H. (1985) Rapidly induced defences and talking trees: the devils’ advocate position. American Naturalist, 126: 181-195.

Green, T.R. & Ryan, C.A. (1972) Wound induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science: 175: 776-777.

Hartley, S.E. & Lawton, J.H. (1987) Effects of different types of damage on the chemistry of birch foliage and the responses of birch feeding insects. Oecologia, 74: 432-437.

Haukioja, E. & Hakala, T. (1975) Herbivore cycles and periodic outbreaks. Report of the Kevo Subarctic Research Station, 12: 1-9

Haukioja, E. & Hanhimäki, S. (1984) Rapid wound induced resistance in white birch (Betula pubescens) foliage to the geometrid Epirrita autumnata: a comparison of trees and moths within and outside the outbreak range of the moth. Oecologia, 65, 223-228.

Haukioja, E. & Niemelä, P. (1976). Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station 13: 44-47.

Haukioja, E. & Niemelä, P. (1977). Retarded growth of a geometrid larva after mechanical damage to leaves of its host tree. Annales Zoologici Fennici 14: 48-52.

Heil, M. & Ton, J. (2008) Long-distance signalling in plant defence. Trends in Plant Science, 13: 264-272.

Karban, R. & Myers, J.H. (1989) Induced plant responses to herbivory. Annual Review of Ecology & Systematics, 20: 331-348.

Leather, S.R., D., W.A., & Forrest, G.I. (1987) Insect-induced chemical changes in young lodgepole pine (Pinus contorta): the effect of previous defoliation on oviposition, growth and survival of the pine beauty moth, Panolis flammea. Ecological Entomology, 12: 275-281.

Mäntyllä, E., Blande, J.D., & Klemola, T. (2014) Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod-Plant Interactions, 8, 143-153.

Michereff, M.F.F., Borges, M., Laumann, R.A., Dinitz, I.R., & Blassioli-Moraes, M.C. (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telonomus podisi. Entomologia experimentalis et applicata, 147: 9-17.

Trewhella, K.E., Leather, S.R., & Day, K.R. (1997) Insect induced resistance in lodgepole pine: effects on two pine feeding insects. Journal of Applied Entomology, 121: 129-136.

Myers, J. H. (1998). Synchrony in outbreaks of forest lepidoptera: a possible example of the Moran effect. Ecology 79: 1111-1117.

Painter, R.H. (1958) Resistance of plants to insects. Annual Review of Entomology, 3: 267-290.

Rhoades, D.F. (1983) Responses of alder and willow to attack by tent caterpillar and webworms: evidence for pheromonal sensitivity of willows. American Chemical Society Symposium Series, 208: 55-68.

Rhoades, D.F. (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. American Naturalist, 125: 205-238.

Ruohomäki, K., Hanhimäki, S., Haukioja, E., Iso-iivari, L., & Neuvonen, S. (1992) Variability in the efficiency of delayed inducible resistanec in mountain birch. Entomologia experimentalis et applicata, 62: 107-116.

Ruohmäki, K., Tanhuanpää, M., Ayres, M.P., Kaitaniemi, P., Tammaru, T. & Haukioja, E. (2000) Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Population Ecology, 42: 211-223

Smith, C.M. & Boyko, E.V. (2007) The molecular basis of plant resistance and defence responses to aphid feeding: current status. Entomologia experimentalis et applicata, 122: 1-16.

Thaler, J. (1999) Induced resistance in agricultural crops: effects of Jasmonic acid on herbivory and yield in tomato plants. Environmental Entomology, 28, 30-37.

Turchin, P., Taylor, A. D. &Reeve, J. D. (1999). Dynamical role of predators in population cycles of a forest insect: an experimental test. Science 285: 1068-1071.

Van Hulten, M., Pelser, M., van Loon, L.C., Pieterse, C.M.J. & Ton, J. (2006) Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences USA, 103: 5602-5607.

 

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3 Comments

Filed under Entomological classics, EntoNotes, Ten Papers That Shook My World, Uncategorized

3 responses to “Ten Papers that Shook My World – Haukioja & Niemelä (1976) – the plant “immune response”

  1. Pingback: Ten Papers that Shook My World – Haukioja & Niemelä (1976) – the plant “immune response” - Todd DeanTodd Dean

  2. Pingback: Ten Papers that Shook My World – Owen & Weigert (1976) – The things that eat you are good for you | Don't Forget the Roundabouts

  3. Pingback: Ten papers that shook my world – Way & Banks (1964) – counting aphid eggs to protect crops | Don't Forget the Roundabouts

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