Gall-Inducing Insects and Plants: the Induction Conundrum
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REVIEW ARTICLE Gall-inducing insects and plants: the induction conundrum Anantanarayanan Raman* CSIRO (Health and Biosecurity), Underwood Avenue, Floreat Park, WA 6014 & Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia rizes what is currently known in the induction of galls, Galls induced by insects and mites (insects, hereafter) have been a subject of interest to insect ecologists simultaneously pointing to the many gaping holes in that because of the unusual habit of gall induction and for knowledge and the areas that need to be focused upon. their tightly connected relationships. These specialist Galls induced by insects (hereafter ‘galls’) exemplify 12–14 insects and mites have been explored to explain the defined plant growth . Plant-growth regulators (PGRs) nature of interactions between them and the plants by were implicated as the key. Nysterakis15,16 demonstrated entomologists, ecologists and plant physiologists over auxins in the salivary extracts of gall-inducing Daktulos- the last two centuries. However, the questions why phaira vitifoliae (Phylloxeridae) on Vitis vinifera (Vita- only certain insect taxa induce galls on specific species ceae) and leaf curl-inducing Brachycaudus helichrysi of plants and how galls are induced remain challeng- (Aphididae) on Prunus domestica var. domestica (Rosa- ing. Whereas several efforts made across the world ceae) by testing with the oat–coleoptile and vine–tendril– implicate plant-growth regulators (PGRs) in answer- spin tests, popular in the 1940s. The inhibitory and hyper- ing the question on how galls are induced, this article emphasizes the establishment of a metaplasied cell at trophic effects on plants with salivary-extract injections were clarified as due to variations in auxin levels17,18. In the location where the tip of the chitinous mandible 17,19 or ovipositor first hits in the plant. In the light of the the D. vitifoliae–V. vinifera gall system, Nysterakis differentiation of a metaplasied cell, the earliest plant related the auxins detected in the saliva of D. vitifoliae to response, it is but critical to evaluate the physiology of auxin precursors in V. vinifera. Boysen–Jensen20 deter- that cell and the ‘new’ physiological events triggered mined that auxins regulate growth in the galls induced by around it, heralding gall initiation. PGRs certainly Mikiola fagi (Cecidomyiidae) on Fagus sylvatica (Faga- play a role in gall growth, but only during later stages. ceae). In the next two decades, Guiscarfé-Arillaga21, This article does not answer the question on how galls Beck22, Nolte23, Leatherdale24 and Schäller25 – to name a are induced. However, it brings to light the gaps that few – obtained ‘swellings’ on plants by injecting meas- need to be addressed in future in the backdrop of the ured quantities of indole-acetic acid (IAA). Such artifi- efforts made over the years. Since we need to deal with the physiological changes that occur in a meta- cially induced swellings were true plant growths, but they plasied cell and a few adjacent cells, the use of sophis- differed from the naturally induced galls because the ticated optical equipment and pertinent software former lacked a definite shape and internal tissue diffe- to achieve a structured and articulate explanation im- rentiation. Bioassay of whole-body extracts (WBEs) of presses as the way to go. insects was a popular method used in implicating 26,27 28,29 IAA . Hori confirmed auxin-like compounds in Keywords: Cell-wall debris, chitinous mandible, gall non-gall-inducing, plant-feeding Miridae, Pentatomidae induction, pathogenic fungi, plant-growth regulators. and Coreidae (Hemiptera) using the WBE method in the 1970s. INSECTS and mites (hereafter ‘insects’) and the galls they Although only indirectly relevant, it would be pertinent induce are known presently far more than before1–4. The to recall the ‘tumour-inducing principle’ (TiP) in Agro- bacterium (Rhizobiaceae)-induced tumours on plants discovery of ‘samurai’ aphids and their unique behaviour 30 among the gall-inducing Aphidoidea by Shigéyûki Aôki proposed by Braun (Rockefeller University, USA) in was a milestone event5,6 that stimulated similar explorations the 1950s. The TiP got explained as the ‘Ti-plasmid’ in other gall-inducing insect groups7. The co-evolutionary edited by an endonuclease in the 1980s. However, many stark differences differentiate an Agrobacterium-induced ecology of gall-inducing insects and their host plants is a 31 widely pursued topic today8–11. Yet, the answer to the tumour from a gall . When much was spoken about the role of IAA and other question on how galls are induced is in a mess. This 32 article focuses on the above elusive question. It summa- plant hormones in galls, Anders detected lysine, histi- dine and tryptophan in higher levels, and glutamic acid and valine in lower levels in the salivary secretions of D. *e-mail: [email protected]; [email protected] vitifoliae. He generated knotty swellings (‘nodosities’) on 66 CURRENT SCIENCE, VOL. 120, NO. 1, 10 JANUARY 2021 REVIEW ARTICLE V. vinifera roots cultured in solutions with measured that a gall is the result of insect action is vital, because quantities of the specified amino acids. Because the gene- other plant abnormalities such as witches’ brooms, fascia- rated swellings were morphologically similar to galls tions, crinkles, folds and puckerings – either vectored by induced by D. vitifoliae on the roots of V. vinifera, insects or induced by microbes – are not. In a gall, the in- Anders implicated these amino acids as the gall-inducing ducing insect lives as a parasite inflicting minimal altera- chemicals; alternatively, they could be the precursors of tions to the physiology of the host and not killing the gall-inducing chemical. Between 1958 and 1961, it. Küster34 constructively aligned the explanation of Anders published several articles reinforcing the role of galls on the proposition made earlier by Friedrich amino acids in gall induction. However, this was chal- Thomas37,p. 513: lenged a decade later by Miles33 (Adelaide University, Australia). ‘Ein Cecidium nenne … gegen den erfahrenen Reiz.’. Galls are more than entomological and botanical A gall – cecidium – is a developmental deviation of the novelties plant induced by a parasite. The word ‘development’ means an active process. When a leaf is either con- A gall is the product of a natural, tight relationship sumed or mined by a caterpillar, a gall does not mani- between specific insects and plants. It is a near-perfect, fest. To establish a gall, active growth in the part of a exquisite expression on a plant in response to insect ac- plant occurs in response to the stimulus from the para- 34 tion (Figure 1). The response pattern of plants to gall- sitic organism. inducing insects varies: some plant taxa are susceptible and an equal number are resistant because of the levels 35,36 A gall is a phenotypic expression that arises because of and types of proteins they include . An understanding perturbation in normal plant growth initiated and stimu- lated by the insect. In the more-evolved insect orders, e.g. Diptera, an individual neonate induces a gall. In the less- evolved orders, e.g. Thysanoptera and Eriophyoidea, in contrast, a population arising from a gravid female contributes to gall development, although initiation is by the feeding action of the gravid female38. The group gall- establishment behaviour, as in the Thysanoptera and Eri- ophyoidea, occurs in some of the gall-inducing Sternorr- hyncha, e.g. Adelgidae39. What clarifies a gall – irrespective of the inducing insect belonging to a more- or less-evolved order – is the insect’s dependence on the plant for nutrition. Therefore, establishment of the tissue of nutrition in the gall, redirection of different primary metabolites and minerals to that tissue, and completion of most segments of the lifecycle of the inducing insect within the gall are crucial in defining it40. Development of a gall can be generalized into the following stages: (i) initiation, (ii) triggering of new differentiation pathways, including establishment of a special tissue for nutrition, with a concurrent inhibition of the normal development, (iii) growth and (iv) ageing and senescence41,42. This explanation has been verified in many galls on various dicotyledons induced by different insect taxa13,43–45. Although each gall is unique in shape, either a radial or bilateral symmetry in external morpho- logy manifests, an aspect that is strongly deficient in microbe-induced tumours46,47. The nematode-induced root knots (e.g. Meloidogyne, Heteroderidae) are Figure 1. Fir cone-like galls induced by Apsylla cistellata (Hemipte- amorphous, similar to microbe-induced tumours in exter- ra: Psylloidea: Aphalaridae: Rhinocolinae) on the vegetative axillary nal morphology, but differ from the latter because they meristems of Mangifera indica (Anacardiaceae). (Inset) Vertical sec- include ‘giant-nurse cells’ nourishing the nematode48. tional view of the gall showing nymphal chambers. For the biology of A. cistellata and gall development, see Raman et al.134. For distribution These cells are structurally and functionally similar to details, see Sharma and Raman68, Burckhardt et al.135. nutritive cells in galls. CURRENT SCIENCE, VOL. 120, NO. 1, 10 JANUARY 2021 67 REVIEW ARTICLE To comprehensively understand how galls are induced, shoot terminals of Jatropha clavuligera (Euphorbiaceae) the critical element will be to examine the physiology of in South-Central America, is also known to occur on sev- the first two stages: initiation and triggering of new diffe- eral unrelated plants both as a gall-inducing taxon and not a rentiation pathways, which involve the formation of sec- gall-inducing taxon55. However, host-specificity tests of in- ondary messengers in response to the signals perceived fested and uninfested shoots of the Bolivian populations of by the plant because of insect action. The PGRs are pro- J. clavuligera and a few allied and co-occurring species of duced during either the late second or the third stage of Jatropha, made in 2017, have clarified that the populations gall development.