Plant development reprogramming by cynipid gall wasp: proteomic analysis

Pawłowski, Tomasz Andrzej; Leśniewska, Joanna; Karolewski, Piotr; Giertych, M.

doi:10.1007/s11738-017-2414-9

Cited by 14 publications

(15 citation statements)

References 63 publications

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“…Taken together these are compatible with cellular export of these chitinases. Other gall wasp genes showing significantly elevated expression in Early stage galls (S6 Table) included a tyrosine-protein phosphatase, eleven carbonic anhydrases (involved in maintenance of pH balance and transport of carbon dioxide by hydration to bicarbonate [105]), venom acid phosphatase, and a glycine N-acyltransferase-like protein. We found no evidence for gall wasp production of plant hormone homologues in the differentially expressed genes, and neither did we detect expression of BmIAO1 (or any close homologue), a gene involved in endogenous insect production of auxin [106].…”

Section: Resultsmentioning

confidence: 99%

“…Proteomic work on leaf galls induced by other oak cynipids ( Cynips and Neuroterus species) identified overproduction of the enzyme S-adenosyl methionine (SAM) synthase in gall tissues [105]. We found four genes encoding the same enzyme to be differentially over-expressed in Growth stage relative to Early stage galls, two of which are only differentially expressed in gall tissues (TRINITY_DN55180_c4_g1 and TRINITY_DN69171_c2_g1).…”

Section: Discussionmentioning

confidence: 98%

“…SAM synthase catalyses the production of SAM from methionine, and the SAM in turn is a substrate for the synthesis of a range of important plant metabolites, including ethylene and polyamines. Possible roles for these metabolites discussed in [105] include a range of processes relevant to gall induction that includes meristem development [125], regulation of Rhizobium -induced root nodulation in legumes [126], organogenesis and fruit maturation [127]. Further work is required to understand the role(s) of these genes in gall tissues.…”

Section: Discussionmentioning

confidence: 99%

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Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

et al. 2019

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Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

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Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

et al. 2019

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“…This would be beneficial for gall morphogenesis and the nutritional requirements of the larvae (Raman, 2011). Although the method by which A. mukaigawae galls accumulate ASN remains unknown, previous studies showed that developing galls may have the ability to mimic the seed and flower development pathway (Schönrogge et al, 2000;Schultz et al, 2019) and reprogram plant development (Pawłowski et al, 2017).…”

Section: Asparagine Proline and Tryptophanmentioning

confidence: 99%

Alteration of free amino acid concentrations in insect galls induced by Andricus mukaigawae (Hymenoptera; Cynipidae)

Yang

Zhu

2020

Ecological Entomology

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1. Insect galls are abnormal plant growths that develop in response to a stimulus provided by a galling insect. The nutrition hypothesis suggests that the concentrations of nutritive compounds in galls are changed to provide optimum nutrition for the larvae and adults of galling insects. 2. To test the nutrition hypothesis, we determined the concentrations of 20 free amino acids in galls and in galled and ungalled twigs of Quercus fabri during the larval and adult stages of Andricus mukaigawae using high‐performance liquid chromatography with ultraviolet–visible detection. 3. At the larval stage, the concentrations of 12 out of 20 amino acids in A. mukaigawae galls were significantly higher than those in galled and ungalled twigs. Asparagine and tryptophan were the most abundant nonessential and essential amino acids, respectively, in A. mukaigawae galls. 4. At the adult stage, the concentrations of most amino acids, except proline, were significantly lower in A. mukaigawae galls than in galled and ungalled twigs. The A. mukaigawae adults may not manipulate amino acid levels because the adults do not feed on galls. The decrease of amino acid levels in adult galls may be viewed as a depletion. 5. The composition of free amino acids in A. mukaigawae galls was significantly different from the composition in galled and ungalled twigs in both the larval and adult stages. 6. Our results may support the nutrition hypothesis. We suggest that a high concentration of proline in A. mukaigawae galls may protect larvae and adults from plant defense responses.

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“…Even more interesting, Hearn (2013) also determined that genes expressed in gall wasp genomes encode plant-cell-walldegrading enzymes that could originate from plant pathogenic bacteria. Pawłowski, Staszak, Karolewski, and Giertych (2017), using a proteomic approach to compare the galls induced by three oak gall species, Cynips quercusfolii, Cynips longiventris, and Neuroterus quercusbaccarum, with non-gall plant tissue in the host plant Quercus robur, described several proteins that could potentially be related to plant gall formation. On the other hand, for non-insect galls, a transcriptomic approach by Olszak et al (2018) showed evidence that galls induced by Plasmodiophora brassicae in Arabidopsis reprogram critical steps of the host cell cycle.…”

Section: The Induction Mechanism Of Plant Galls By Insects: What Do Wmentioning

confidence: 99%

The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction

Gätjens-Boniche

2019

RBT

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Galls are defined as modifications of the normal developmental design of plants, produced by a specific reaction to the presence and activity of a foreign organism. Although different organisms have the ability to induce galls in plants, insect-induced galls are the most elaborate and diverse. Some hypotheses have been proposed to explain the induction mechanism of plant galls by insects. The most general hypothesis suggests that gall formation is triggered by the action of chemical substances secreted by the gall inducer, including plant growth regulators such as auxins, cytokinins, indole-3-acetic acid (IAA), and other types of compounds. However, the mode of action of these chemical substances and the general mechanism by which the insect could control and manipulate plant development and physiology is still not known. Moreover, resulting from the complexity of the induction process and development of insect galls, the chemical hypothesis is very unlikely a complete explanation of the mechanism of induction and morphogenesis of these structures. Previous and new highlights of insect gall systems with emphasis on the induction process were analyzed on the basis of the author’s integrated point of view to propose a different perspective of gall induction, which is provided in this article. Due to the extraordinary diversity of shapes, colors, and complex structures present in insect galls, they are useful models for studying how form and structure are determined at the molecular level in plant systems. Furthermore, plant galls constitute an important source of material for the study and exploration of new chemical substances of interest to humans, due to their physiological and adaptive characteristics. Considering the finely tuned control of morphogenesis, structural complexity, and biochemical regulation of plant galls induced by insects, it is proposed that an induction mechanism mediated by the insertion of exogenous genetic elements into the genome of plant gall cells could be involved in the formation of this kind of structure through an endosymbiotic bacterium.

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Plant development reprogramming by cynipid gall wasp: proteomic analysis

Cited by 14 publications

References 63 publications

Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

Alteration of free amino acid concentrations in insect galls induced by Andricus mukaigawae (Hymenoptera; Cynipidae)

The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction

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