The mechanism of gall induction makes galls red

Connor, Edward F.; Bartlett, Linnea; O'Toole, Sean; Byrd, Steven; Biskar, Kevin; Orozco, Jessica

doi:10.1007/s11829-012-9210-7

Cited by 35 publications

(40 citation statements)

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“…To date, the only definitive evidence of a role for CKs in the proliferation of gall tissue in plants exists for bacteria [4,25,[39][40][41]. However, CKs have long been implicated as contributing to the formation of the covering gall in fungi [11,12,42,43] and insects [15,16,19,[44][45][46][47][48][49][50]. By covering gall, we mean the plant tissue that envelopes the gall-inducing organism.…”

Section: Introductionmentioning

confidence: 99%

“…Among fungi and insects that encounter senescing plant tissues, some species appear to employ CKs to induce yellowing plant tissues to "stay green" by the process of forming "green islands"-areas of photosynthetically active tissues in which the pathogenic organism can continue to feed and develop [17,[51][52][53][54][55][56][57]. In some instances, CKs have been shown to convert the site of attack into a mobilizing sink to which sugars are translocated where they may contribute to gall induction or just for the sustenance of the manipulating organism [18,28,45,[58][59][60].…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, there is good evidence that a range of plant antagonists, Plants 2020, 9,208 3 of 23 such as bacteria, viruses, fungi, and insects-mainly leaf miners and gall inducers-produce CKs to facilitate invading the plant, perhaps in part by counteracting plant defensive responses [61]. Finally, exogenous CKs, in the presence of light, appear to modify biosynthesis of flavonoids and anthocyanins via altered regulation of the phenylpropanoid pathway, resulting in the synthesis of red and purple pigments that sometimes color the infection site or gall and that may also increase the production of tannins and lignins [45,[63][64][65].…”

Section: Introductionmentioning

confidence: 99%

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Cytokinins Are Abundant and Widespread among Insect Species

Andreas

Kisiała

Emery

et al. 2020

Plants

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Cytokinins (CKs) are a class of compounds that have long been thought to be exclusively plant growth regulators. Interestingly, some species of phytopathogenic bacteria and fungi have been shown to, and gall-inducing insects have been hypothesized to, produce CKs and use them to manipulate their host plants. We used high performance liquid chromatography-electrospray ionization tandem mass spectrometry (HPLC-MS/MS) to examine concentrations of a wide range of CKs in 17 species of phytophagous insects, including gall- and non-gall-inducing species from all six orders of Insecta that contain species known to induce galls: Thysanoptera, Hemiptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera. We found CKs in all six orders of insects, and they were not associated exclusively with gall-inducing species. We detected 24 different CK analytes, varying in their chemical structure and biological activity. Isoprenoid precursor nucleotide and riboside forms of trans-zeatin (tZ) and isopentenyladenine (iP) were most abundant and widespread across the surveyed insect species. Notably, the observed concentrations of CKs often markedly exceeded those reported in plants suggesting that insects are synthesizing CKs rather than obtaining them from the host plant via tissue consumption, compound sequestration, and bioaccumulation. These findings support insect-derived CKs as means for gall-inducing insects to manipulate their host plant to facilitate cell proliferation, and for both gall- and non-gall-inducing insects to modify nutrient flux and plant defenses during herbivory. Furthermore, wide distribution of CKs across phytophagous insects, including non-gall-inducing species, suggests that insect-borne CKs could be involved in manipulation of source-sink mechanisms of nutrient allocation to sustain the feeding site and altering plant defensive responses, rather than solely gall induction. Given the absence of any evidence for genes in the de novo CK biosynthesis pathway in insects, we postulate that the tRNA-ipt pathway is responsible for CK production. However, the unusually high concentrations of CKs in insects, and the tendency toward dominance of their CK profiles by tZ and iP suggest that the tRNA-ipt pathway functions differently and substantially more efficiently in insects than in plants.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cytokinins Are Abundant and Widespread among Insect Species

Andreas

Kisiała

Emery

et al. 2020

Plants

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“…Auxins regulate a vast array of plant processes including growth and development as well as responses to light, gravity, abiotic stress, and pathogen attack (Glick, 2015;Mano and Nemoto, 2012;Yang et al, 2014). Several studies suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation, since some gall-forming herbivores contain high levels of IAA Davies, 2001a, 2001b;Tooker and de Moraes, 2011a;Straka et al, 2010;Dorchin et al, 2009;Yamaguchi et al, 2012;Tanaka et al, 2013), IAA pools and signaling are enhanced in parasitized plant tissue (Yamaguchi et al, 2012;Tooker and de Moraes, 2011b), and direct application of IAA can result in the formation of gallresembling structures (Hamner and Kraus, 1937;Guiscafrearrillaga, 1949;Schäller, 1968;Bartlett and Connor, 2014;Connor et al, 2012). In the context of chewing insects, however, our understanding is more limited (Dafoe et al, 2013).…”

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confidence: 99%

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

et al. 2016

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Plant responses to herbivore attack are regulated by phytohormonal networks. To date, the role of the auxin indole-3-acetic acid (IAA) in this context is not well understood. We quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary metabolism. We found that IAA is strongly, rapidly, and specifically induced by herbivore attack. IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes. IAA accumulation starts 30 to 60 s after local induction and peaks within 5 min after induction, thereby preceding the jasmonate (JA) burst. IAA accumulation does not require JA signaling and spreads rapidly from the wound site to systemic tissues. Complementation and transport inhibition experiments reveal that IAA is required for the herbivore-specific, JA-dependent accumulation of anthocyanins and phenolamides in the stems. In contrast, IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool diterpene glycosides in the same tissue. Taken together, our results uncover IAA as a rapid and specific signal that regulates a subset of systemic, JA-dependent secondary metabolites in herbivore-attacked plants.

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“…Although, in general terms, it has been accepted that some kind of "chemical stimuli" (very likely a phytohormone) from the insect is involved in the induction and morphogenesis of galls (McCalla et al, 1961;Miles, 1968;Rohfritsch & Shorthouse, 1982;Hori, 1992;Leitch, 1994;Ananthakrishnan, 1998;Raman, 2011;Yamaguchi et al, 2012;Connor et al, 2012;Erb, Meldau & Howe, 2012;Giron et al, 2013, Tooker & Helms, 2014Bailey et al, 2015;Oates et al, 2016, Giron et al, 2016, up to now it has not been possible to determine with certainty whether insects could synthesize phytohormones. However, Yamaguchi et al (2012) found abnormally high concentrations of a type of zeatine in the glands of the "sawfly" Pontania sp.…”

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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The mechanism of gall induction makes galls red

Cited by 35 publications

References 73 publications

Cytokinins Are Abundant and Widespread among Insect Species

Cytokinins Are Abundant and Widespread among Insect Species

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

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

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