Tag Archives: symbionts

Green Islands – mining cytokinins

A little while ago I wrote about the phenomenon of  “green islands” caused by ants keeping insect herbivores away from trees.   If, however, you work on leaf miners, the term green islands means something else entirely.  Instead of referring to a feature of the landscape, it refers to a feature of the leaf, which unless you are Toby*, is definitely not a landscape-level phenomenon 😊

While some insects, aphids for example, induce senescence to improve the quality of their host plant and some plants induce senescence and early leaf-fall in those leaves that have been colonised by gall aphids in order to reduce their infestation load (Williams & Whitham, 1986), there are other insects that try desperately to prevent senescence so as to prolong their feeding life on what would otherwise be a dead leaf.

Green island leaf mine of the moth, Stigmella atricapatella – Many thanks to Mike Shurmer for the photographs.

The phenomenon of the green islands in autumn leaves associated with leaf mining Lepidoptera has been known about for some time (Hering, 1951), but although the adaptive value of this was easy to see, the causal mechanism remained unknown for some time. Similarly, plant pathologists had also noticed that one of the symptoms of powdery mildew infections is the appearance of a green ring around the necrotic spot caused by the fungus (von Tubeuf, 1897); if not a green island, a green atoll 😊

Green island or green atoll? Powdery mildew on wheat https://slideplayer.com/slide/9073461/27/images/14/Green+island+on+wheat+infected+with+wheat+powdery+mildew.jpg

That fungi produced secretions containing plant growth substances such as the auxin (plant hormones) indole acetic acid has been known since the 1930s (Thimann, 1935) and it was later hypothesised that the levels present in the surrounding leaf tissue were associated with the resistance or lack thereof, to the fungal agent (e.g. Shaw & Hawkins, 1958). A further class of plant growth substances, initially termed kinins because of their similarity to kinetin (a cell growth promoting plant hormone, but later renamed cytokinins** (Skoog et al., 1965)) were discovered by Folke Skoog and co-workers (Miller et al., 1956) and linked to the production of green islands by plant pathogens (reviewed by Skoog & Armstrong, 1970).

“What about the leaf miners?” I hear you ask. You will be pleased to know that entomologists were not too far behind. Lisabeth Engelbrecht working on Nepticulid leaf miners on birch (Betula pendula) and Aspen (Populus tremula) set up a study (Engelbrecht, 1968) to test her hypothesises that the green islands were caused as a result of insect saliva or by the larvae physically cutting the leaf veins that would otherwise have delivered the chemical signal responsible for beginning leaf senescence. She discovered that the green islands contained large concentrations of cytokinin  (Engelbrecht, 1968) and working with other colleagues discovered that the labial glands of leaf mining larvae also contained cytokinin, but was unsure as to whether the cytokinin originated from the larvae or were formed in the leaf in response to chemicals in the saliva or frass of the larvae (Engelbrech et al., 1969), although if you read the paper it is quite clear that she is convinced that the source of the cytokinin is from the larvae and not the plant.

After all this excitement about insect produced cytokinin and green islands things seemed to go a bit dead.  I found a couple of passing references to the possibility that leaf mining Lepidopteran larvae use cytokinin to produce a green island to extend larval life after leaf abscission (Miller, 1973; Faeth, 1985) and an opinion piece discussing the possible adaptive role of using green islands to prolong larval life after leaf fall (Kahn & Cornell, 1983), but, surprisingly, nothing experimental to test this hypothesis. Oddly, I did find a paper testing the idea that early leaf abscission was an induced defence against leaf miners, where green islands were mentioned in the introduction but not mentioned again (Stiling & Simberloff, 1989).

Don’t get me wrong, plant pathologists and entomologists working on insect galls were still writing about the role of cytokinin (e.g. Murphy et al., 1997: Mapes & Davies, 2001), but leaf miner green island research seemed to have died.  Suddenly, however, in the mid-2000s the French ‘discovered’ leaf miners and David Giron and colleagues, showed how the leaf miner Phyllonorycer blancardella manipulates the nutritional quality of their host leaves by increasing the levels of cytokinin in the surrounding leaf tissue (Giron et al., 2007).

‘Green island’ formed by Phyllonorycter blancardella (From Giron et al., 2007).

 

As we know from aphids, where insects play, bacterial symbionts are never far away, and sure enough it wasn’t long before it was shown that Wolbachia ‘infections’ were helping the leaf miners produce their ‘green islands’. Wilfried Kaiser and colleagues treated leaf miner larvae with antibiotics to remove the symbiont and found that the ‘cured’ larvae, although still able to feed and form leaf mines, were unable to produce ‘green islands’ and the levels of cytokinin were much lower than that found in the ‘green islands’ formed by untreated leaf miners (Kaiser et al., 2010).

Influence of Wolbachia on green island formation. To the left, infected leaf miners (Phyllonorycter blancardella) happily surrounded by nutritious plant tissue; to the right, ‘cured’ by antibiotics, the leaf miner soon runs out of food (Kaiser et al., 2010)

The same group have also documented the mechanism by which the leaf miners and their symbionts work together (Body et al., 2013) and also, using molecular phylogenies and ecological trait data, shown that the existence of the ‘green island’ phenotype and Wolbachia infections are associated with the evolutionary diversification of the Gracillarid leaf miners (Gutzwiller et al., 2015).

You might expect that these findings would have stimulated renewed interest in the ‘green island’ phenomenon, but you would be wrong.  Despite the fact that at the time of writing this article (September 10th 2019) Kaiser et al. (2010) had, according to the Web of Science, been cited 105 times, only three papers dealing with this phenomenon have been published, the most recent appearing in early 2018 (Zhang et al., 2018) and, incidentally, by the same group that published the Kasier et al. (2010) study. It would appear that as with ‘green islands’, the study of the phenomenon is also very localised.

References

Allen, P.J. (1942) Changes in the metabolism of wheat leaves induced by infection with powdery mildew. American Journal of Botany, 42, 425-435.

Body, M., Kaiser, W., Dubreuil, G., Casas, J. & Giron, D. (2013) Leaf-miners co-opt microorganisms to enhance their nutritional environment. Journal of Chemical Ecology, 39, 969-977.

Engelbrecht, L. (1968) Cytokinin in den ,,grunen Inseln” des Herbstlauibes. Flora oder Allgemeine botanische Zeitung. Abt. , Physiologie und Biochemie, 159, S, 208-214.

Englebrecht , L., Orban, U. & Heese, W. (1969) Leaf-miner caterpillars and cytokinins in the “green islands” of autumn leaves. Nature, 223, 319-321.

Faeth, S.H. (1985) Host leaf selection by leaf miners: interactions among three trophic levels. Ecology, 66, 870-875.

Gutzwillner, F., Dedeine, F., Kaiser, W., Giron, D., & Lopez-Vaamonde, C. (2015) Correlation between the green-island phenotype and Wolbachia infections during the evolutionary diversification of Gracillariidae leaf-mining moths. Ecology & Evolution, 5, 4049-4062.

Hering, E.M. (1951) Biology of the Leaf Miners, Dr W Junk, The Hague, Netherlands

Herrick, G.W. (1922) The Maple Case-Bearer Paraclemensia Acerifoliella Fitch. Journal of Economic Entomology, 15, 282-288.

Kahn, D.M. & Cornell, H.V. (1983) Early leaf abscission and folivores: comments and considerations. American Naturalist, 122, 428-432.

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, 277, 2311-2319.

Mapes, C.C. & Davies, P.J. (2001) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytologist, 151, 203-212.

Miller, C. O., Skoog, F., Okumura, F. S., Von Saltza, M. H., & Strong, F. M. (1956). Isolation, structure and synthesis of Kinetin, a substance promoting cell division. Journal of the American Chemical Society, 78, 1375–1380.

Miller, P.F. (1973) The biology of some Phyllonorycter species (Lepidoptera: Gracillariidae) mining leaves of oak and beech. Journal of Natural History, 7, 391-409.

Murphy, A.M., Pryce-Jones, E., Johnstone, K. & Ashby, A.M. (1997) Comparison of cytokinin production in vitro by Pyrenopeziza brassicae with other plant pathogens. Physiological & Molecular Plant Pathology, 50, 53-65.

Shaw, M. & Hawkins, A.R. (1958) the physiology of host-parasite relations V. A preliminary examination of the level of free endogenous Indoleacetic acid in rusted and mildewed cereal leaves and their ability to decarboxylate exogenously supplied radioactive indoleacetic acid. Canadian Journal of Botany, 34, 389-405.

Skoog, F. & Armstrong, D.J. (1970) Cytokinins. Annual Review of Plant Physiology, 21, 359-384.

Skoog, F., Strong, F.M. & Miller, C.O. (1965) Cytokinins. Science, 148, 532-533.

Stiling, P.D. & Simberloff, D. (1989) Leaf abscission – induced defense against pests or response to damage ? Oikos, 55, 43-49.

Thimann, K.V. (1935) On the plant growth hormone produced by Rhizopus suinus. Journal of Biological Chemistry, 109, 279-291.

Von Tubeuf, K.F. (1897) Diseases of Plants, Longmans, Green & Co, London.

Walters, D.R., McRoberts, N. & Fitt, B.D.L. (2008) Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biological Reviews, 83, 79-102.

Williams, A.G. & Whitham, T.G. (1986) Premature leaf abscission: an induced plant defense against aphids. Ecology, 67, 1619-1627.

Zhang,  H., Dubreuil, G., Faivre, N., Dobrev, P., Kaiser, W., Huguet, E., Vankova, R. & Giron, D.  (2018) Modulation of plant cytokinin levels in the Wolbachia‐free leaf‐mining species Phyllonorycter mespilella. Entomologia experimentalis et applicata, 166, 428-438.

 

*Toby Alone (La Vie Suspendue) by Timothée de Fombelle, is a fantastic novel, which I only fairly recently discovered, but can heartily recommend.

** Cytokinins are a class of plant growth substances that promote cell division, or cytokinesis, in plant roots and shoots. They are involved primarily in cell growth and differentiation, but also affect apical dominance, axillary bud growth, and leaf senescence. Wikipedia

 

 

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Not all aphids have the same internal biomes

Headline message for those of you too busy to read the whole thing

Aphids have mutualistic symbiotic bacteria living inside them, one set, the primary endosymbionts, Buchnera aphidicola are obligate, i.e. in normal circumstances, the aphid can’t live without them and vice versa. All aphids have them. The others, the secondary symbionts, of which there are, at the last count, more than seven different species, are facultative, i.e. aphids can survive without them and not all aphids have them or the same combination of them. These can help the aphid in many ways, such as, making them more resistant to parasitic wasps, able to survive heat stress better and helping them use their host plants more efficiently. Hosting the secondary symbionts may, however, impose costs on the aphids.

Now read on, or if you have had enough of the story get back to work  🙂

Like us, aphids have a thriving internal ecology, they are inhabited by a number of bacteria or bacteria like organisms. The existence of these fellow travellers and the fact that they are transmitted transovarially, has been known for over a hundred years (Huxley, 1858; Peklo, 1912)*, although their role within the body of the aphids was not entirely understood for some time, despite Peklo’s conviction that they were symbionts and transferred via the eggs to the next generation. Some years later the Hungarian entomologist László Tóth** hypothesised that aphids because the plant sap that they feed on did not contain enough proteins to meet their demands for growth, must be obtaining the extra nitrogen they needed from their symbionts, although he was unable to prove this empirically (Tóth, 1940). This was very firmly disputed by Tom Mittler some years later, who using the giant willow aphid, Tuberolachnus salignus, showed that aphid honeydew and willow phloem sap contained the same amino acids (Mittler, 1953, 1958ab). It was not only aphidologists who were arguing about the nature and role of insect symbionts, as this extract from a review of the time makes clear,

It is not our purpose here to harangue on terminology; suffice it to say that we will use “symbiote” for the microorganism and “host” for the larger organism (insect) involved in a mutualistic or seemingly mutualistic association.” (Richards & Brooks, 1958).

Interestingly it is in this paper that they mention, using the term “provocactive” the use of antibiotics to create aposymbiotic individuals in attempts to prove that the symbionts were first bacteria, and second, benefiting their insect hosts. The concluded that there was enough evidence to suggest that the endosymbionts were involved in some way in the nutritional and possibly reproductive processes of the insects studied, mainly cockroaches. At the time of the review no similar work had been done on aphids. A few years later though, two American entomologists sprayed aphids with several different antibiotics and found that this caused increased mortality and reduced fecundity when compared with untreated ones (Harries & Mattson, 1963). Presaging its future dominance in aphid symbiont work, one of the aphids was the pea aphid, Acyrthosiphon pisum. Antibiotics were also shown to eliminate and damage the symbionts associated with Aphis fabae followed by impaired development and fecundity in the aphid itself adding yet more evidence that the symbionts were an essential part of the aphid biome (Ehrhardt & Schmutterer, 1966). There was, however, still much debate as to how the symbionts provided proteins to the aphids, and although light and electron microscopy studies confirmed that the symbionts were definitely micro-organisms (Lamb & Hinde, 1967; Hinde, 1971), the answer to that question was to remain unanswered until the 1980s although the development of aphid artificial diets (Dadd & Krieger, 1967) which could be used in conjunction with antibiotic treatments, meant that it was possible to show that the symbionts provided the aphids with essential amino acids (Dadd & Kreiger, 1968; Mittler, 1971ab).*** Although the existence of secondary symbionts in other Homoptera was known (Buchner, 1965), it was not until Rosalind Hinde described them from the rose aphid, Macrosiphum rosae, that their presence in aphids was confirmed (Hinde, 1971).   Of course it was inevitable that they would then be discovered in the pea aphid although their role was unknown (Grifiths & Beck, 1973). Shortly afterwards they were able to show that material produced from the symbionts was passed into the body of the aphid (Griffiths & Beck, 1975) and it was also suggested suggested that it was possible that the primary symbionts were able to synthesise amino acids (Srivastava & Auclair, 1975) and sterols (Houk et al., 1976) for the benefit of their aphid hosts (partners). By the early 1980s it was accepted dogma that aphids were unable to reproduce or survive without their primary symbionts (Houk & Griffiths, 1980; Ishikawa, 1982) and by the late 1980s that dietary sterols were provided by the primary symbionts (Douglas, 1988).

Symbionts

Primary symbiont (P) in process of dividing seen next to secondary symbionts (S) and mitochondrion (m) from Houk & Griffiths (1980).

Despite the huge amount of research and the general acceptance that the endosymbionts were an integral part of the aphid’s biome “The mycetocyte symbionts are transmitted directly from one insect generation to the next through the female. There are no known cases of insects that acquire mycetocyte symbionts from the environment or from insects other than their parents” (Douglas , 1989), their putative identity was not determined until 1991 (Munson et al., 1991), when they were named Buchnera aphidicola, and incidentally placed in a brand new genus. Note however, that like some aphids, B. aphidicola represents a complex of closely related bacteria and not a single species (Moran & Baumann, 1994). Research on the role of the primary symbionts now picked up pace and it was soon confirmed that they were responsible for the synthesis of essential amino acids used by the aphids, such as tryptophan (Sasaki et al., 1991; Douglas & Prosser, 1992) and that it was definitely an obligate relationship on both sides**** (Moran & Baumann, 1994).

Now that the mystery of the obligate primary endosymbionts was ‘solved’, attention turned to the presumably facultative secondary symbionts, first noticed more than twenty years earlier (Hinde, 1971)***** began to be scrutinised in earnest. Nancy Moran and colleagues (Moran et al., 2005) identified three ‘species’ of secondary bacterial symbionts, Serratia symbiotica, Hamiltonella defensa and Regiella insecticola. As these are not found in all individuals of a species they are facultative rather than obligate. The secondary symbionts were soon shown not to have nutritional benefits for the aphids (Douglas et al., 2006). They are instead linked to a whole swathe of aphid life history attributes, ranging from resistance to parasitoids (Oliver et al., 2003; 2005; Schmid et al., 2012), resistance to heat and other abiotic stressors (Montllor et al., 2002; Russell & Moran 2006; Enders & Miller, 2016) and to host plant use (Tsuchida et al., 2004; McLean et al., 2011; Zytynska et al., 2016).

And finally, Mittler (1971b) mentions the reddish colouration developed by aphids reared on some of the antibiotic diets and hypothesises that this may be linked to the symbionts. I have written earlier about aphid colour variants and the possibility that the symbionts may have something to do with it. The grain aphid, Sitobion avenae has a number of colour variants and it was suggested that levels of carotenoids present might have something to do with the colours expressed and that in some way this was controlled by the presence of absence of symbionts (Jenkins et al., 1999). More recently Tsuchida and colleagues in a series of elegant experiments on the ubiquitous pea aphid, have shown that the intensity of green colouration is dependent on the presence of yet another endosymbiont, a Rickettsiella (Tsuchida et al., 2010). The authors hypothesise that being green

Pea aphids colour

Elegant demonstration that in some strains of the pea aphid, green colour is a sign of an infection by Rickettsiella (Tsuchida et al., 2010).

rather than pink or red, may reduce predation by ladybirds as has been suggested before (Losey et al., 1997).

New secondary symbionts continue to be discovered and with each discovery, new hypotheses are raised and tested. It would seem that there is a whole ecology of secondary symbionts within the aphid biome waiting to be explored and written about (Zytynska & Weisser, 2016). What are you waiting for, but do remember to come up for air sometime and relate what you find back to the ecology of the aphids 🙂

 

References

Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York.

Dadd, R.H. & Krieger, D.L. (1967) Continuous rearing of aphids of the Aphis fabae complex on sterile synthetic diet. Journal of Economic Entomology, 60, 1512-1514.

Dadd, R.H. & Krieger, D.L. (1968) Dietary amino acid requirements of the aphid Myzus persicae. Journal of Insect Physiology, 14, 741-764.

Douglas, A.E. (1988) On the source of sterols in the green peach aphid, Myzus persicae, reared on holidic diets. Journal of Insect Physiology, 34, 403-408.

Douglas, A.E. (1998) Mycetocyte symbiosis in insects. Biological Reviews, 64, 409-434.

Douglas, A.E. & Prosser, W.A. (1992) Sythesis of the essential amiono acid trypthotan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38, 565-568.

Douglas, A.E., Francois, C.M.L.J. & Minto, L.B. (2006) Facultative ‘secondary’ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiological Entomology, 31, 262-269.

Ehrhardt, P. & Schmutterer, H. (1966) Die Wirkung Verschiedener Antibiotica auf Entwicklung und Symbionten Künstlich Ernährter Bohnenblattläuse (Aphis fabae Scop.). Zeitschrift für Morphologie und Ökologie der Tiere, 56, 1-20.

Enders, L.S. & Miller, N.J. (2016)Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid. Ecology & Evolution, 6, 818-829.

Griffiths, G.W. & Beck, S.D. (1973) Intracellular symbiotes of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 19, 75-84.

Griffiths, G.W. & Beck, S.D. (1975) Ultrastructure of pea aphid mycetocystes: evidence for symbiote secretion. Cell & Tissue Research, 159, 351-367.

Harries, F.H. & Mattson, V.J. (1963) Effects of some antibiotics on three aphid species. Journal of Economic Entomology, 56, 412-414.

Hinde, R. (1971) The control of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. Journal of Insect Physiology, 17, 1791-1800.

Houk, E.J. & Griffiths, G.W. (1980) Intracellular symbiotes of the Homoptera. Annual Review of Entomology, 25, 161-187.

Houk, E.J., Griffiths, G.W. & Beck, S.D. (1976) Lipid metabolism in the symbiotes of the pea aphid, Acyrthosiphon pisum. Comparative Biochemistry & Physiology, 54B, 427-431.

Huxley, T.H. (1858) On the agamic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society of London, 22, 193-219.

Ishikawa, H. (1978) Intracellular symbionts as a major source of the ribosomal RNAs in the aphid mycetocytes. Biochemical & Biophysical Research Communications, 81, 993-999.

Ishikawa, H. (1982) Isolation of the intracellular symbionts and partial characterizations of their RNA species of the elder aphid, Acyrthosiphon magnoliae. Comparative Biochemistry & Physiology, 72B, 239-247.

Jenkins,  R.L., Loxdale, H.D., Brookes, C.P. & Dixon, A.F.G. (1999)  The major carotenoid pigments of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae).  Physiological Entomology, 24, 171-178. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-3032.1999.00128.x/pdf

Lamb, R.J. & Hinde, R. (1967) Structure and development of the mycetome in the cabbage aphid, Brevicoryne brassciae. Journal of invertebrate Pathology, 9, 3-11.

Losey, J. E., Ives, A. R., Harmon, J., Ballantyne, F. &Brown, C. (1997). A polymorphism maintained by opposite patterns of parasitism and predation. Nature, 388, 269-272.

McLean, A.H.C., van Asch, M., Ferrari, J. & Godfray, H.C.J. (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B., 278, 760-766.

Mittler, T.E. (1953) Amino-acids in phloem sap and their excretion by aphids. Nature, 172, 207.

Mittler, T.E. (1958a) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. Journal of Experimental Biology, 35, 74-84.

Mittler, T.E. (1958b) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). III The nitrogen economy. Journal of Experimental Biology, 35, 626-638.

Mittler, T.E. (1971a) Dietary amino acid requirements of the aphid Myzus persicae affected by antibiotic uptake. Journal of Nutrition, 101, 1023-1028.

Mittler, T.E. (1971b) Some effects on the aphid Myzus persicae of ingesting antibiotics incorporated into artificial diets. Journal of Insect Physiology, 17, 1333-1347.

Montllor, C.B., Maxmen, A. & Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea pahids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.

Moran, N. & Baumann, P. (1994) Phylogenetics of cytoplasmically inherited microrganisms of arthropods. Trends in Ecology & Evolution, 9, 15-20.

Moran, N.A., Russell, J.A., Koga, R. & Fukatsu, T. (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied & Environmental Microbiology, 71, 3302-3310.

Munson, M.A., Baumann, P. & Kinsey, M.G. (1991) Buchnera gen. nov. and Buchnera aphidicola sp. Nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. International Journal of Systematic Bacteriology, 41, 566-568.

Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences USA, 100, 1803-1807.

Oliver, K.M., Moran, N.A. & Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences USA, 102, 12795-12800.

Peklo, J (1912) Über symbiotische Bakterien der Aphiden. Berichte der Deutschen Botanischen Gesellschaft, 30, 416-419.

Richards, A.G. & Brooks, M.A. (1958) Internal symbiosis in insects. Annual Review of Entomology, 3, 37-56.

Russell, J.A. & Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B, 273, 603-610.

Sasaki, T., Hayashi, H. & Ishikawa, H. (1991) Growth and reproduction of the symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum mainatained on artificial diets. Journal of Insect Physiology, 37, 749-756.

Schmid, M., Sieber, R., Zimmermann, Y.S. & Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26, 207-215.

Srivastava P.N. & Auclair, J.L. (1975) Role of single amino acids in phagostimualtion, growth, and survival of Acyrthosiphon pisum. Journal of Insect Physiology, 21, 1865-1871.

Tóth, L. (1940) The protein metabolism of aphids. Annales Musei Nationalis Hungarici 33, 167-171.

Tsuchida, T., Koga, R. & Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989.

Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., Simon, J. C. &Fukatsu, T. (2010). Symbiotic bacterium modifies aphid body color. Science 330: 1102-1104.

Zytynska, S. E. &Weisser, W. W. (2016). The natural occurrence of secondary bacterial symbionts in aphids. Ecological Entomology, 41, 13-26.

Zytynska, S.E., Meyer, S.T., Sturm, S., Ullmann, W., Mehrparvar, M. & Weisser, W.W. (2016) Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia, 180, 735-747.

 

Footnotes

*I should point out that although Huxley clearly described the structure and contents of the mycetocytes he had absolutely no idea what they were and what function, if any, they had. Despite the many authors who supported Peklo’s claim that the contents of the mycetocytes were bacteria he was still having to defend himself against detractors more than 50 years later (Peklo, 1953).

Peklo, J. (1953) Microorganisms or mitochondria? Science, 118, 202-206.

 

**not to be confused with the László Tóth who vandalised Michelangelo’s Pietà

***interestingly, although the existence of primary symbionts in aphids and their possible role in aphid nutrition was by then firmly established, my vade mecum as a student, Tony Dixon’s Biology of Aphids, makes no mention of them at all, although first published in 1973. The first edition of Aphid Ecology (1985) also by Tony Dixon, only devotes three quarters of a page to them, but by the second edition, published in 1998, they get a whole chapter to themselves.

Buchnera appears to have been ‘lost’ but replaced by a yeast like symbiont (Braendle et al., (2003).

Braendle, C., Miura, T., Bickel, R., Shingleton, A.W., Kambhampari, S. & Stern, D.L. (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PloS Biology, 1, e21. doi:10.1371/journal.pbio.0000021.

 

*****although Huxley’s description of the unknown structures that he saw in aphids in 1858, does seem to include secondary symbionts as well as the primary ones.

Glossary

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Do pea aphids rule the world? Joint UK-French Aphid Meeting Paris

Last week (5th to 6th November 2015) I had the great privilege and pleasure to attend an aphid conference in Paris – my favourite insects and my favourite city – heaven!  The conference was mainly organised by our French colleagues from INRA, under the direction of Jean-Christophe Simon with help from Richard Harrington, recently retired from Rothamsted Research, and a tiny bit of input from me.

The meeting was held at the Societe Nationale D’Horticulture De France, a building cunningly hidden away down a long passageway off the Rue de Grenelle which debuts into a small courtyard where I found the main entrance and was reassured by the sight of the

Venue

organisers feverishly getting name tags ready (I was very early as had thought it would take longer to walk there than it actually did) and

Notice

a suitably amusingly appropriate sign on the door.

I was greeted enthusiastically by Jean-Christophe, caused a bit of a hiatus by having to have my name badge located and was then pointed gently, but firmly at the coffee 🙂

The rest of the delegates began to arrive some twenty minutes later or so and shortly after we were ushered into the lecture theatre, which was very full.

Lecture

After getting over the shock of being told that there was no Wifi available (that put paid to my plans for Tweeting), I settled down to enjoy the morning. The conference began with an invited presentation from Takema Fukatsu from Japan who gave us an overview on symbiosis, evolution and biodiversity.   This was then followed by two shorter talks of 12.5 minutes each leading us into the first coffee break.  One of the great things about this conference was, that apart from the plenary presentation, all talks were restricted to 10 minutes with 2.5 minutes for questions.  This meant that we got to hear 40 (yes forty) talks over the two days and that we had refreshment breaks every 75 minutes, (the coffee was excellent).  The refreshment breaks were half an hour long, and lunch was an hour, thus giving delegates plenty of time to mix and chat about their work.

There were just over a 100 delegates coming from eight different countries, although as one might expect, most were from France and the UK. It was great to see so many people working on aphids, although not all could be described as “aphidologists” sensu stricto, but I am sure that everyone there would be happy to be included under that description as sensu lato 🙂 Sadly in the UK the number of aphidologists has declined greatly since I was a student, especially those working on their ecology and morphotaxonomy.

The focus of the talks and posters, of which there were 21, was predominantly on the interactions of aphids with their host plants and natural enemies. The role of symbionts in these interactions and the molecular mechanisms involved was especially highlighted, in particular those involved with the pea aphid, Acyrthosiphon pisum.  Aproximately 40% of the talks were on the pea aphid, and a further 28% on the most pestiferous aphid in the world, Myzus persicae and its ability to develop resistance to pesticides.  Although I find aphid symbionts fascinating, I am a bit concerned that they and the pea aphid seem to be taking over the world!  Given the number of talks, I am not going to review them all.   For those interested the full programme and abstracts can be found here.  Highlights for me were Christoph Vorburger from ETH who gave an entertaining talk about the effect that endosymbionts have in protecting aphids against parasitoids, and making me feel old, Ailsa McLean from Oxford University, whom I first met when she was in her pram (she is the daughter of Ian Mclean with whom I shared a lab when we were PhD students).  I was also very pleased to be chairing the session in which Charles Dedryver (now retired) was speaking about the history of aphidology.  I was less happy that I had to cut his talk short, but my duties left me no other choice 🙂  Despite Charles and I exchanging reprints for almost 40 years, this was the first time that we had ever come face to face.

All in all a fantastic conference and many congratulations to the team from INRA for organising it so well. My one concern, which I touched upon earlier was the predominance of the pea aphid as a model organism and the overriding focus on the molecular aspects of the various interactions.  I find it a little worrying that I can find statements in papers such as “This is an exciting time for pea aphid biologists”  (Brisson, 2010), which hardly indicates a broad viewpoint. As a further indication of an overly narrow focus, during the breaks it was noticeable that of the people who ventured outside, I was the only one turning leaves over and looking for aphids, the others were indulging their nicotine habits.

Aphids

It is important that as aphidologists, entomologists and ecologists we do not lose sight of the big picture.

 

Reference

Brisson, J.A. (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philosophical Transactions of the Royal Society B, 365, 60-616

 

Sensu stricto in the narrow sense; Sensu lato broadly speaking

 

A non-entomological post script

The added bonus of having the conference in Paris was that my wife had an excuse to pop over for the weekend and I was able to extend my visit. The weather was fantastic and we had a great time eating, drinking and seeing as many sights as we could fit in.  Luckily the weather was glorious.

Cafe Gourmand

My favourite sort of pudding – Café Gourmand (at Le Café Gourmand)

We rode the funicular to the top of Montmartre, something which despite having visited Paris at least once a year for the last 15 years or so, we had never done. Then after visiting the Montmartre Museum, we walked down to the cemetery.  Paris has some great cemeteries and we never miss the chance to see what curiosities we can find.

Dr Pitchal

A psychoanalyst with a macabre sense of humour Dr. Guy Pitchal (1922-1989), Psychoanalyst known for working with many French celebrities — including the singer Dalida, who is buried nearby.

Nijinsky

The Great Nijinsky – looking a bit fed-up?

Zola

Emile Zola – we came across his magnificent tomb entirely by accident, after taking a wrong flight of stairs.

La Goulue

Cancan dancer extraordinaire, La Goulue (The Glutton).

Moped inventor

Robert Mayet – Inventor of the moped

Looking for somewhere to eat on Saturday evening we came across a number of shops already preparing for Christmas.

Polar bears

Christmas will apparently soon be with us!

Bees Gare du Nord

Bees get everywhere – no idea what this was about but saw it as we were heading for the Eurostar.

 

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