Feeding and Other Gall Facets: Patterns and Determinants in Gall Structure
TL;DR: The animal-induced galls have a striking anatomical diversity, concerning several patterns, which were reunited herein, and culminates in extant gall structural diversity.
Abstract: Galls are neoformed structures induced by specific animals, fungi, bacteria, virus or some parasitic plants on their host plant organs. Developmental processes are well known in Agrobacterium tumefasciens galls, but the animal-induced galls have a striking anatomical diversity, concerning several patterns, which were reunited herein. Anatomical traits observed in animal-induced galls involve manipulation of plant morphogenesis in convergent ways. Nematode, mite and insect galls usually contain homogeneous storage parenchyma and develop due to hyperplasia and cell hypertrophy. The development of typical nutritive tissues, giant cells, or hypertrophied vascular bundles may occur. Some other anatomical features may be usually restricted to galls induced by specific taxa, but they may eventually be related to the developmental potentialities of the host plants. The combination of distinct morphogenetic peculiarities in each gall system culminates in extant gall structural diversity. Convergent anatomical traits are observed according to the feeding mode of the gall inducers, representing potentiation or inhibition of similar events of host plant morphogenesis and cell redifferentiation, independent of gall-inducing taxa.
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01 Jan 1980
TL;DR: The histopathogenesis of the foliar galls induced by Nothanguina phyllobia Thorne in Solanum elaeagnilolium Cav. was examined via serial sections prepared from plant shoots at 11 time intervals (0.5-30 days) following inoculation as mentioned in this paper.
Abstract: The histopathogenesis of the foliar galls induced by Nothanguina phyllobia Thorne in Solanum elaeagnilolium Cav. was examined via serial sections prepared from plant shoots at 11 time intervals (0.5-30 days) following inoculation. Nematodes infected the blades and petioles of young leaves surrounding the shoot apex. Hypertrophy and hyperplasia of the palisade, pith, cortical, and vascular parenchyma resulted in the formation of confluent leaf, petiole, and stem galls up to 25 cm(3) in volume. Externally, leaf galls were irregular, light-green, convoluted spheroid bulges distending the abaxial surface. Mature galls contained a cavity lined with parenchymogenous nutritive tissue comprising intercellular spaces and actively dividing hypertrophied cells. These cells contained granular cytoplasm, hypertrophied nuclei, and brightly stained large nucleoli. Vascular tissues were not discernibly affected during the early stages of gall development. As gall development progressed, however, vascular elements were often displaced and disoriented. The histopathology of this nematode indicates that N. phyllobia is a highly specialized parasite and, for that reason, is suitable as a biological control agent.
15 citations
TL;DR: Despite their analogous functionalities, the protoplast and cell wall features of TNT cells of nematode galls and of the feeding cells of the Eriophyidae galls are distinct, and work out through different strategies toward keeping gall developmental site active.
Abstract: Cell walls and protoplast may work together or distinctly in the establishment of the functional profiles of gall tissue compartments. This presumption is herein evaluated in three gall systems by immunocytochemical and ultrastructural analyses. The common storage tissues (CSTs) of leaf galls induced by Eriophyidae on Miconia ibaguensis leaves and by Ditylenchus gallaeformans on M. ibaguensis and M. albicans have rigid and porous cell walls due to their composition of pectins. Hemicelluloses in CST cell walls are scarcer when compared to the cell walls of the control leaves, being functionally compensated by rigid pectate gels. The typical nutritive tissues (TNTs) in galls induced by Ditylenchus gallaeformans are similar to promeristematic and secretory cells regarding their enriched cytoplasm, several mitochondria, and proplastids, as well as multivesicular and prolamellar bodies in cell membranes. The cytological features of the feeding cells of Eriophyidae galls indicate that they are not as metabolically active as the cells of the TNT in nematode galls. However, their cell wall composition suggests more plasticity and porosity than the cells of the TNT, which can compensate the less production of nutrients with more transport. The ultrastructural and immunocytochemical profiles of CST cells reveal functional similarities, which are independent of the taxa of the gall inducer or of the host plant. Despite their analogous functionalities, the protoplast and cell wall features of TNT cells of nematode galls and of the feeding cells of the Eriophyidae galls are distinct, and work out through different strategies toward keeping gall developmental site active.
13 citations
Cites background from "Feeding and Other Gall Facets: Patt..."
...Nevertheless, these epidermal cells do not constitute a TNT, even though they accumulate reducing sugars (Ferreira et al. 2017a, 2019b)....
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...The cells of the TNTs have granulose and dense cytoplasm, an evident nucleus, indicating intense metabolic activity (Kostoff and Kendall 1929; Bronner 1992; Ferreira et al. 2017a, 2019a)....
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...They may accumulate lipids, reducing sugars and/or proteins, depending on the parasite and host plant species (Oliveira et al. 2010; Ferreira and Isaias 2013, 2014; Ferreira et al. 2017a, 2019a, b; Isaias et al. 2018)....
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...Anatomical studies have revealed the compartmentalization of tissues and functions in galls (Bragança et al. 2017; Ferreira et al. 2017a, 2019a; Isaias et al. 2018)....
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...The distinct phenotypes of the host plants also influence the metabolic responses of the gall systems studied herein (Ferreira et al. 2019a)....
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TL;DR: Reducing sugars in the TNT are important for the production of new cell walls during the indeterminate growth of the galls, which have increased levels of water-soluble polysaccharides that corroborate such hypothesis.
Abstract: The galls induced by Ditylenchus gallaeformans (Nematoda) on leaves of Miconia albicans have unique features when compared to other galls. The nematode colonies are surrounded by nutritive tissues with promeristematic cells, capable of originating new emergences facing the larval chamber, and providing indeterminate growth to these galls. Considering enzyme activity as essential for the translocation of energetic molecules from the common storage tissue (CST) to the typical nutritive tissue (TNT), and the major occurrence of carbohydrates in nematode galls, it was expected that hormones would mediate sink strength relationships by activating enzymes in indeterminate growth regions of the galls. Histochemical, immunocytochemical and quantitative analyses were made in order to demonstrate sites of enzyme activity and hormones, and comparative levels of total soluble sugars, water soluble polysaccharides and starch. The source-sink status, via carbohydrate metabolism, is controlled by the major accumulation of cytokinins in totipotent nutritive cells and new emergences. Thus, reducing sugars, such as glucose and fructose, accumulate in the TNT, where they supply the energy for successive cycles of cell division and for nematode feeding. The histochemical detection of phosphorylase and invertase activities indicates the occurrence of starch catabolism and sucrose transformation into reducing sugars, respectively, in the establishment of a gradient from the CST towards the TNT. Reducing sugars in the TNT are important for the production of new cell walls during the indeterminate growth of the galls, which have increased levels of water-soluble polysaccharides that corroborate such a hypothesis. Functional relationship between plant hormone accumulation, carbohydrate metabolism and cell differentiation in D. gallaeformans-induced galls is attested, providing new insights on cell development and plant metabolism.
9 citations
TL;DR: Although cell wall dynamics is peculiar to each gall morphotype in Inga ingoides, the role of xyloglucans as carbohydrate reserve to the gall inducers constitutes a functional trait common the three morphotypes.
Abstract: The intriguing questions concerning gall development refer to the processes of the remodelling of the host plant organ. Such processes involve the restructuring of cell walls and can be influenced by phenolics, indole-3-acetic acid (IAA) and reactive oxygen species (ROS). Alterations in cell walls demand the interference in the coupling of cellulose fibrils and hemicelluloses (xyloglucans) at specific stages of gall development. In addition to cell wall remodelling, hemicelluloses, such as the, xyloglucans and heteromannans can act as reserve carbohydrates, while xylans provide rigidity to the secondary cell walls. Developmental traits of the lenticular, fusiform and globoid galls on Inga ingoides (Fabaceae) were analysed using anatomical, cytometric, histochemical and immunocytochemical tools. Phenolics, IAA and ROS accumulated in similar gall tissue compartments, and may have influenced the restructuring of hemicelluloses and pectins. Contrary to expectations, cell wall flexibility regarding the dynamics of xyloglucans and cellulose fibrils does not relate to a temporal scale. The detection of xyloglucans in nutritive cell walls relate to carbohydrate nutritional resources to the galling insect, while xylans were associated to the lignified cell walls. Heteromanans were not detected, either in non-galled or galled tissues. The patterns of cell expansion during gall development relied on the relationship among phenolics, ROS and IAA with the hemicelluloses (xyloglucans and xylans) and cellulose fibrils. Although cell wall dynamics is specific to each gall morphotype in I. ingoides, the xyloglucans function as carbohydrate reserve to the gall inducers, which constitutes a functional trait common to the three morphotypes.
8 citations
TL;DR: A review of current knowledge on gall induction by fig wasps and exposes the many lacunae in this area can be found in this paper, which makes connections between fig and gall-inducing wasp traits, and suggests relatively unexplored research avenues.
Abstract: The ancient interaction between figs (Ficus, Moraceae) and their pollinating fig wasps is an unusual example of a mutualism between plants and gall-inducing insects. This review intends to offer fresh perspectives into the relationship between figs and the diversity of gall-inducing sycophiles which inhabit their enclosed globular inflorescences that function as microcosms. Besides gall-inducing pollinators, fig inflorescences are also inhabited by other gall-inducing wasps. This review evaluates the state of current knowledge on gall-induction by fig wasps and exposes the many lacunae in this area. This review makes connections between fig and gall-inducing wasp traits, and suggests relatively unexplored research avenues. This manuscript calls for an integrated approach that incorporates such diverse fields as life-history theory, plant mate choice, wasp sexual selection and local mate competition, plant embryology as well as seed and fruit dispersal. It calls for collaboration between researchers such as plant developmental biologists, insect physiologists, chemical ecologists and sensory biologists to jointly solve the many valuable questions that can be addressed in community ecology, co-evolution and species interaction biology using the fig inflorescence microcosm, that is inhabited by gall-inducing mutualistic and parasitic wasps, as a model system.
6 citations
References
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TL;DR: The mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions are described and the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
Abstract: Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxified by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genome-wide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
9,908 citations
"Feeding and Other Gall Facets: Patt..." refers background in this paper
...The ROS are captured by cinnamyl alcohols (precursors of lignins) and immobilized when deposited in cell walls (Barceló, 1997; Apel & Hirt, 2004)....
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Book•
13 Oct 2005
TL;DR: This work focuses on the development of the Plant Body-An Overview of the Protoplast, which consists of the Plasma Membrane, Nucleus, and Cytoplasmic Organelles, and its surrounds.
Abstract: Preface. Acknowledgments. General References. Chapter 1. Structure and Development of the Plant Body-An Overview. Chapter 2. The Protoplast: Plasma Membrane, Nucleus, and Cytoplasmic Organelles. Chapter 3. The Protoplast: Endomembrane System, Secretory Pathways, Cytoskeleton, and Stored Compounds. Chapter 4. Cell Wall . Chapter 5. Meristems and Differentiation. Chapter 6. Apical Meristems. Chapter 7. Parenchyma and Collenchyma. Chapter 8. Sclerenchyma. Chapter 9. Epidermis. Chapter 10. Xylem: Cell Types and Developmental Aspects. Chapter 11. Xylem: Secondary Xylem and Variations in Wood Structure. Chapter 12. Vascular Cambium. Chapter 13. Phloem: Cell Types and Developmental Aspects. Chapter 14. Phloem: Secondary Phloem and Variations in Its Structure. Chapter 15. Periderm. Chapter 16. External Secretory Structures. Chapter 17. Internal Secretory Structures. Addendum: Other Pertinent References Not Cited in the Text. Glossary. Author Index. Subject Index.
994 citations
TL;DR: It is suggested that the hypothesis that selection imposed by enemies remains the most probable adaptive explanation for the evolution of diversity in insect galls has yet to be tested explicitly, and the requirements for an appropriate cross-species analysis are discussed.
Abstract: Insect galls are dramatic examples of extended phenotypes: although composed of host plant tissues, their development is largely controlled by insect genes. Adaptive explanations for gall traits should thus be expressed in terms of impacts on insect fitness, but the extent to which interspecific variation in gall structure is adaptive, and the possible selective pressures driving diversification in gall form remain controversial. In colonial aphids and thrips, gall structures probably diversified in response to selection for enhancement of the surface area available for feeding. In other taxa, such as gall wasps and gall midges, diversity is expressed predominantly in non-nutritive tissues, particularly those on the gall surface. All natural enemies attack the occupants of closed galls by penetrating gall tissue, and modifications that reduce enemy attack rates should thus be favoured. Recent studies of intraspecific variation in gall form strongly support a defensive role for several traits, but, to date, there is little empirical support for enemies as a cause of interspecific variation in gall form. Selection imposed by enemies nevertheless remains the most probable adaptive explanation for the evolution of diversity. We suggest that this hypothesis has yet to be tested explicitly, and discuss the requirements for an appropriate cross-species analysis.
708 citations
"Feeding and Other Gall Facets: Patt..." refers background in this paper
...Among the holometabolous, the Diptera: Cecidomyiidae and Hymenoptera: Cynipidae induce the most diverse galls (Espírito-Santo & Fernandes, 2007), which are histologically and histochemically peculiar (Wells, 1920; Rohfritsch, 1992; Harris, 1994; Stone & Schonrögge, 2003; Ferreira & Isaias, 2014)....
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...The galls are usually species-specific structures, and their anatomy and metabolism are strongly related to the gall inducer species and to the host plants (Stone & Schonrögge, 2003; Moura et al., 2008; Carneiro et al., 2015; Ferreira et al., 2017b, 2018)....
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...The sclerenchymatic cells may also provide mechanical protection for the gall inducers against natural enemies in maturation phase (Stone & Schonrögge, 2003; Carneiro et al., 2014b)....
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...The increment of indumentum may occur in several gall systems (Ferreira et al., 2017a), and is usually related to the protection of the gall-inducing agent against abiotic stresses and natural enemies, even though these effects must be tested (Stone & Schonrögge, 2003)....
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...These secondary metabolites are supposed to function as protective barriers against excessive sun radiation and UV light (Dias et al., 2013a, 2013b; Bragança et al., 2017), as well as against the natural enemies of the galling organism (Stone & Schonrögge, 2003; Bragança et al., 2017)....
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TL;DR: The evolution of the galling habit has followed two pathways, one via mining plant tissues and the other from sedentary external herbivores that then modify plant growth.
Abstract: Major hypotheses on the adaptive significance of insect gall formation are reviewed: nonadaptive, plant protection, mutual benefit, nutrition, microenvironment, and enemy hypotheses. We evaluate the validity of each, and find the first three to be without merit because galls clearly have adaptive features for the insect, but few if any for the plant, and the galler has negative impact on the plant, making the relationship parasitic. Predictions are developed to enable testing of hypotheses, and tests are discussed. Nutrition and microenvironment hypotheses are supported, while the enemy hypothesis remains with several uncertain issues to be resolved. The evolution of the galling habit has followed two pathways, one via mining plant tissues and the other from sedentary external herbivores that then modify plant growth. In each route the sequence of selective factors was probably different, but improved protection from hygrothermal stress and improved nutrition are of primary importance, and protection from enemies probably reinforced the galling habit.
514 citations
"Feeding and Other Gall Facets: Patt..." refers background in this paper
...Gall anatomical structure may protect the gall inducers against natural enemies and unfavorable environmental conditions (Price et al., 1987; Fernandes & Price, 1992; Stone & Schonrögge, 2003)....
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TL;DR: The hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution is proposed.
Abstract: Summary
1. Although secondary metabolites are recognized as fundamental to the defence of plants against insect and mammalian herbivores, their relative importance compared to other potential defensive plant traits (e.g. physical resistance, gross morphology, life-history, primary chemistry and physiology) are not well understood.
2. We conducted a meta-analysis to answer the question: What types of genetically variable plant traits most strongly predict resistance against herbivores? We performed a comprehensive literature search and obtained 499 separate measurements of the strength of covariation (measured as genetic correlations) between plant traits and herbivore susceptibility – these were extracted from 72 studies involving 19 plant families.
3. Surprisingly, we found no overall association between the concentrations of secondary metabolites and herbivore susceptibility – plant traits other than secondary metabolites most strongly predicted herbivore susceptibility. Specifically, genetic variation in life-history traits (e.g. flowering time, growth rate) consistently exhibited the strongest genetic correlations with susceptibility. Genetic variation in gross morphological traits (e.g. no. branches, plant size) and physical resistance traits (e.g. latex, trichomes) were also frequently correlated with variation in herbivore susceptibility, but these relationships depended on attributes of the herbivores (e.g. feeding guild) and plants (e.g. longevity).
4. These results call into question the conventional wisdom that secondary metabolites are the most important anti-herbivore defence of plants. We propose the hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution. Meanwhile, secondary metabolites could have evolved to be important defensive mechanisms not because they have the largest effect on herbivores, but because the constraints on their evolution are the weakest.
452 citations
"Feeding and Other Gall Facets: Patt..." refers background in this paper
...A dense indumentum is usually related to the increment of a boundary layer in plants, which ends up decreasing the transpiration rates and reflecting the excessive light, as well as increasing the defenses against herbivores (Schreuder et al., 2001; Carmona et al., 2011)....
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