Artificial Light for Improving Tomato Recovery Following Grafting: Transcriptome and Physiological Analyses.

Grafting is widely used to enhance the phenotypic traits of tomatoes, alleviate biotic and abiotic stresses, and control soil-borne diseases of the scion in greenhouse production. There are many factors that affect the healing and acclimatization stages of seedlings after grafting. However, the role of light has rarely been studied. In this study, we compared the effects of artificial light and traditional shading (under shaded plastic-covered tunnels) on the recovery of grafted tomato seedlings. The results show that the grafted tomato seedlings recovered using artificial light had a higher healthy index, leaf chlorophyll content, shoot dry weight, and net photosynthetic rate (Pn) and water use efficiency (WUE) compared with grafted seedling recovered using the traditional shading method. Transcriptome analysis showed that the differentially expressed genes (DEGs) of grafted seedlings restored using artificial light were mainly enriched in the pathways corresponding to plant hormone signal transduction. In addition, we measured the endogenous hormone content of grafted tomato seedlings. The results show that the contents of salicylic acid (SA) and kinetin (Kin) were significantly increased, and the contents of indoleacetic acid (IAA) and jasmonic acid (JA) were decreased in artificial-light-restored grafted tomato seedlings compared with those under shading treatments. Therefore, we suggest that artificial light affects the morphogenesis and photosynthetic efficiency of grafted tomato seedlings, and it can improve the performance of tomato seedlings during grafting recovery by regulating endogenous hormone levels.

Increased gene expression variability hinders the formation of regional mechanical conflicts leading to reduced organ shape robustness.

To relate gene networks and organ shape, one needs to address two wicked problems: i) Gene expression is often variable locally, and shape is reproducible globally; ii) gene expression can have cascading effects on tissue mechanics, with possibly counterintuitive consequences for the final organ shape. Here, we address such wicked problems, taking advantage of simpler plant organ development where shape only emerges from cell division and elongation. We confirm that mutation in VERNALIZATION INDEPENDENCE 3 (VIP3), a subunit of the conserved polymerase-associated factor 1 complex (Paf1C), increases gene expression variability in Arabidopsis. Then, we focused on the Arabidopsis sepal, which exhibits a reproducible shape and stereotypical regional growth patterns. In vip3 sepals, we measured higher growth heterogeneity between adjacent cells. This even culminated in the presence of negatively growing cells in specific growth conditions. Interestingly, such increased local noise interfered with the stereotypical regional pattern of growth. We previously showed that regional differential growth at the wild-type sepal tip triggers a mechanical conflict, to which cells resist by reinforcing their walls, leading to growth arrest. In vip3, the disturbed regional growth pattern delayed organ growth arrest and increased final organ shape variability. Altogether, we propose that gene expression variability is managed by Paf1C to ensure organ robustness by building up mechanical conflicts at the regional scale, instead of the local scale.

RHO GTPase of plants regulates polarized cell growth and cell division orientation during morphogenesis.

Cell polarity-broadly defined as the asymmetric distribution of cellular activities and subcellular components within a cell-determines the geometry of cell growth and division during development. RHO GTPase proteins regulate the establishment of cell polarity and are conserved among eukaryotes. RHO of plant (ROP) proteins are a subgroup of RHO GTPases that are required for cellular morphogenesis in plants. However, how ROP proteins modulate the geometry of cell growth and division during the morphogenesis of plant tissues and organs is not well understood. To investigate how ROP proteins function during tissue development and organogenesis, we characterized the function of the single-copy ROP gene of the liverwort Marchantia polymorpha (MpROP). M. polymorpha develops morphologically complex three-dimensional tissues and organs exemplified by air chambers and gemmae, respectively. Mprop loss-of-function mutants form defective air chambers and gemmae, indicating ROP function is required for tissue development and organogenesis. During air chamber and gemma development in wild type, the MpROP protein is enriched to sites of polarized growth at the cell surface and accumulates at the expanding cell plate of dividing cells. Consistent with these observations, polarized cell growth is lost and cell divisions are misoriented in Mprop mutants. We propose that ROP regulates both polarized cell growth and cell division orientation in a coordinated manner to orchestrate tissue development and organogenesis in land plants.

"Pathomorphogenic" Changes Caused by Citrus Bark Cracking Viroid and Transcription Factor TFIIIA-7ZF Variants Support Viroid Propagation in Tobacco.

Viroids are small, non-coding, pathogenic RNAs with the ability to disturb plant developmental processes. This dysregulation redirects the morphogenesis of plant organs, significantly impairing their functionality. Citrus bark cracking viroid (CBCVd) causes detrimental developmental distortions in infected hops (Humulus lupulus) and causes significant economic losses. CBCVd can infect cells and tissues of the model plant tobacco (Nicotiana tabacum), provided it is delivered via transgenesis. The levels of CBCVd in tobacco were enhanced in plant hybrids expressing CBCVd cDNAs and either the tobacco or hop variant of TFIIIA-7ZF, a viroid-mediated splicing derivative of transcription factor IIIA, which is important for viroid replication by DNA-dependent RNA polymerase II. The TFIIIA-7ZF variants can change the tobacco morphogenesis if expressed in leaves and shoots. In addition to the splitting of shoots, the "pathomorphogenic" network in hybrid plants expressing CBCVd and HlTFIIIA-7ZF induced leaf fusions and malformations. Moreover, CBCVd can dramatically change another morphogenesis into teratomic and petal-like tissues if propagated above some limit in young transgenic tobacco microspores and anthers. By comparative RNA profiling of transgenic tobacco shoots bearing TFIIIA-7ZFs and CBCVd-transformed/infected anthers, we found a differential expression of many genes at p < 0.05. As the main common factor showing the differential up-regulation in shoot and anther tissues, a LITTLE ZIPPER 2-like transcription factor was found. We propose that this factor, which can interact as a competitive inhibitor of the also dysregulated homeobox-leucin zipper family protein (HD-ZIPIII) in apical meristem, is essential for a network responsible for some morphological changes and modifications of plant degradome within shoot meristem regulation and secondary xylem differentiation.

Primary Cell Wall Modifying Proteins Regulate Wall Mechanics to Steer Plant Morphogenesis.

Plant morphogenesis involves multiple biochemical and physical processes inside the cell wall. With the continuous progress in biomechanics field, extensive studies have elucidated that mechanical forces may be the most direct physical signals that control the morphology of cells and organs. The extensibility of the cell wall is the main restrictive parameter of cell expansion. The control of cell wall mechanical properties largely determines plant cell morphogenesis. Here, we summarize how cell wall modifying proteins modulate the mechanical properties of cell walls and consequently influence plant morphogenesis.

Shaping the Organ: A Biologist Guide to Quantitative Models of Plant Morphogenesis.

Organ morphogenesis is the process of shape acquisition initiated with a small reservoir of undifferentiated cells. In plants, morphogenesis is a complex endeavor that comprises a large number of interacting elements, including mechanical stimuli, biochemical signaling, and genetic prerequisites. Because of the large body of data being produced by modern laboratories, solving this complexity requires the application of computational techniques and analyses. In the last two decades, computational models combined with wet-lab experiments have advanced our understanding of plant organ morphogenesis. Here, we provide a comprehensive review of the most important achievements in the field of computational plant morphodynamics. We present a brief history from the earliest attempts to describe plant forms using algorithmic pattern generation to the evolution of quantitative cell-based models fueled by increasing computational power. We then provide an overview of the most common types of "digital plant" paradigms, and demonstrate how models benefit from diverse techniques used to describe cell growth mechanics. Finally, we highlight the development of computational frameworks designed to resolve organ shape complexity through integration of mechanical, biochemical, and genetic cues into a quantitative standardized and user-friendly environment.

A Life Cycle for Modeling Biology at Different Scales.

Modeling has become a popular tool for inquiry and discovery across biological disciplines. Models allow biologists to probe complex questions and to guide experimentation. Modeling literacy among biologists, however, has not always kept pace with the rise in popularity of these techniques and the relevant advances in modeling theory. The result is a lack of understanding that inhibits communication and ultimately, progress in data gathering and analysis. In an effort to help bridge this gap, we present a blueprint that will empower biologists to interrogate and apply models in their field. We demonstrate the applicability of this blueprint in two case studies from distinct subdisciplines of biology; developmental-biomechanics and evolutionary biology. The models used in these fields vary from summarizing dynamical mechanisms to making statistical inferences, demonstrating the breadth of the utility of models to explore biological phenomena.

The term "caline" in plant developmental biology.

In the 1930s, Frits Warmolt Went conducted a number of seminal studies on pea seedlings that had been germinated in the dark and assessed their growth when either the apical parts, cotyledons, or roots were cut off or grafted, to assess whether coplant growth factors assisted auxin in the development of these organs. Went assigned the term "calines" to all auxin-assisting substances, specifically rhizocaline, caulocaline, and phyllocaline in root, shoot (and axillary buds) and leaf development, respectively. Those experiments were based exclusively on growth assays, and no supplementary biochemical or physiological analyses were ever conducted, and additional proof was only provided by Went using pea or tomato. The lack of independent reproducibility by other groups, combined with the fact that the hormonal control of these developmental events in plants is now fairly well-studied event, even at the molecular level, suggests that these growth factors that Went observed 80 years ago either do not exist or are known by some other term in modern plant development. The terms related to "calines" should thus no longer be used in plant developmental biology.

Arabidopsis CURLY LEAF functions in leaf immunity against fungal pathogens by concomitantly repressing SEPALLATA3 and activating ORA59.

Arabidopsis non-host resistance against non-adapted fungal pathogens including Colletotrichum fungi consists of pre-invasive and post-invasive immune responses. Here we report that non-host resistance against non-adapted Colletotrichum spp. in Arabidopsis leaves requires CURLY LEAF (CLF), which is critical for leaf development, flowering and growth. Microscopic analysis of pathogen behavior revealed a requirement for CLF in both pre- and post-invasive non-host resistance. The loss of a functional SEPALLATA3 (SEP3) gene, ectopically expressed in clf mutant leaves, suppressed not only the defect of the clf plants in growth and leaf development but also a defect in non-host resistance against the non-adapted Colletotrichum tropicale. However, the ectopic overexpression of SEP3 in Arabidopsis wild-type leaves did not disrupt the non-host resistance. The expression of multiple plant defensin (PDF) genes that are involved in non-host resistance against C. tropicale was repressed in clf leaves. Moreover, the Octadecanoid-responsive Arabidopsis 59 (ORA59) gene, which is required for PDF expression, was also repressed in clf leaves. Notably, when SEP3 was overexpressed in the ora59 mutant background, C. tropicale produced clear lesions in the inoculated leaves, indicating an impairment in non-host resistance. Furthermore, ora59 plants overexpressing SEP3 exhibited a defect in leaf immunity to the adapted Colletotrichum higginsianum. Since the ora59 plants overexpressing SEP3 did not display obvious leaf curling or reduced growth, in contrast to the clf mutants, these results strongly suggest that concomitant SEP3 repression and ORA59 induction via CLF are required for Arabidopsis leaf immunity to Colletotrichum fungi, uncoupled from CLF's function in growth and leaf development.

A Sight on Single-Cell Transcriptomics in Plants Through the Prism of Cell-Based Computational Modeling Approaches: Benefits and Challenges for Data Analysis.

Single-cell technology is a relatively new and promising way to obtain high-resolution transcriptomic data mostly used for animals during the last decade. However, several scientific groups developed and applied the protocols for some plant tissues. Together with deeply-developed cell-resolution imaging techniques, this achievement opens up new horizons for studying the complex mechanisms of plant tissue architecture formation. While the opportunities for integrating data from transcriptomic to morphogenetic levels in a unified system still present several difficulties, plant tissues have some additional peculiarities. One of the plants' features is that cell-to-cell communication topology through plasmodesmata forms during tissue growth and morphogenesis and results in mutual regulation of expression between neighboring cells affecting internal processes and cell domain development. Undoubtedly, we must take this fact into account when analyzing single-cell transcriptomic data. Cell-based computational modeling approaches successfully used in plant morphogenesis studies promise to be an efficient way to summarize such novel multiscale data. The inverse problem's solutions for these models computed on the real tissue templates can shed light on the restoration of individual cells' spatial localization in the initial plant organ-one of the most ambiguous and challenging stages in single-cell transcriptomic data analysis. This review summarizes new opportunities for advanced plant morphogenesis models, which become possible thanks to single-cell transcriptome data. Besides, we show the prospects of microscopy and cell-resolution imaging techniques to solve several spatial problems in single-cell transcriptomic data analysis and enhance the hybrid modeling framework opportunities.

Nutations in Plant Shoots: Endogenous and Exogenous Factors in the Presence of Mechanical Deformations.

We present a three-dimensional morphoelastic rod model capable to describe the morphogenesis of growing plant shoots driven by differential growth. We discuss the evolution laws for endogenous oscillators, straightening mechanisms, and reorientations to directional cues, such as gravitropic reactions governed by the avalanche dynamics of statoliths. We use this model to investigate the role of elastic deflections due to gravity loading in circumnutating plant shoots. We show that, in the absence of endogenous cues, pendular and circular oscillations arise as a critical length is attained, thus suggesting the occurrence of an instability triggered by exogenous factors. When also oscillations due to endogenous cues are present, their weight relative to those associated with the instability varies in time as the shoot length and other biomechanical properties change. Thanks to the simultaneous occurrence of these two oscillatory mechanisms, we are able to reproduce a variety of complex behaviors, including trochoid-like patterns, which evolve into circular orbits as the shoot length increases, and the amplitude of the exogenous oscillations becomes dominant.

Morphogenic Regulators and Their Application in Improving Plant Transformation.

Generation of plant lines with transgene or edited gene variants is the desired outcome of transformation technology. Conventional DNA-based plant transformation methods are the most commonly used technology but these approaches are limited to a small number of plant species with efficient transformation systems. The ideal transformation technologies are those that allow biotechnology applications across wide genetic background, especially within elite germplasm of major crop species. This chapter will briefly review key regulatory genes involved in plant morphogenesis with a focus on in vitro somatic embryogenesis and their application in improving plant transformation.

Alternatively spliced BobCAL transcripts alter curd morphotypes in a collection of Chinese cauliflower accessions.

The curd of cauliflower (Brassica oleracea L. var. botrytis) is a modified inflorescence that is consumed as a vegetable. Curd formation is proposed to be due to a mutation in the BobCAULIFLOWER (BobCAL) gene, but the genetic relationship between BobCAL variation and curd morphotypes remains obscure. To address this question, we collected and classified a collection of 78 cauliflower accessions into four subpopulations according to curd surface features: smooth, coarse, granular, and hairy curd morphotypes. Through the cDNA sequencing of BobCAL alleles, we showed that smooth and coarse accessions characterized by inflorescence meristem arrest presented a strong association with the 451T SNP (BobCAL_T), whereas granular and hairy accessions marked with floral organ arrest presented an association with 451G (BobCAL_G). Interestingly, all BobCAL alleles were alternatively spliced, resulting in a total of four alternative splice (AS) variants due to the retention of the fourth and/or seventh introns. Among accessions with BobCAL_G alleles, the total expression of all these AS variants in granular plants was almost equal to that in hairy plants; however, the expression of the individual AS variants encoding intact proteins relative to those encoding truncated proteins differed. Hairy accessions showed relatively high expression of the individual variants encoding intact proteins, whereas granular accessions displayed relatively low expression. In smooth cauliflower, the overexpression of the BobCAL_Ga variant caused an alteration in the curd morphotype from smooth to hairy, concurrent with an increase in the expression levels of downstream floral identity genes. These results reveal that alternative splicing of BobCAL transcripts is involved in the determination of cauliflower curd morphotypes.

Gibberellin induced shot berry formation in cv. Early Sweet is a direct consequence of high fruit set.

The 'seedless' table grape industry relies mainly on stenospermocarpic cultivars, in which endosperm abortion results in berries with seed rudiments and low levels of bioactive gibberellin (GA). Application of GA to enhance berry sizing in these cultivars is often accompanied by adverse effects, one of which is increased proportions of very small berries (termed shot berries). Manual removal of these berries, which is essential to improve uniformity and market value, increases production cost and exposes the cluster to damage. Unraveling the physiological causes of shot berry formation is thus of both scientific and practical value. This study focuses on understanding the GA-mediated regulation of shot berry formation in Vitis vinifera cv. Early Sweet, known for a high proportion of shot berries, which severely damage cluster appearance. As GA is known to induce the parthenocarpic fruit set, we first tested the assumption that the parthenocarpic nature of a fruitlet is a primary cause for shot berry development. We then examined the consequence of the flower load on the proportion of shot berries in the cluster. Our data suggests that: (1) contrary to prior assumptions, the parthenocarpic nature of a fruitlet is not the primary cause for shot berry development, demonstrated by the fact that parthenocarpic fruitlets develop into a full-size berries; (2) the proportion of shot berries on a cluster is a function of the initial flower load on the inflorescence, with high initial flower load resulting in greater shot berry percentage in the cluster; (3) GA treatment bypasses the natural regulation of flower load, resulting in high fruitlet density and increased competition among fruitlets; (4) variation of flower load within the cluster influences berry size uniformity to a greater extent than does the variation in number of cluster per vine. The identity of the factors that determine the fate of a given flower on a high-load cluster remains an open question.

The hook shape of growing leaves results from an active regulatory process.

The rachis of most growing compound leaves observed in nature exhibits a stereotypical hook shape. In this study, we focus on the canonical case of Averrhoa carambola. Combining kinematics and mechanical investigation, we characterize this hook shape and shed light on its establishment and maintenance. We show quantitatively that the hook shape is a conserved bent zone propagating at constant velocity and constant distance from the apex throughout development. A simple mechanical test reveals non-zero intrinsic curvature profiles for the rachis during its growth, indicating that the hook shape is actively regulated. We show a robust spatial organization of growth, curvature, rigidity, and lignification, and their interplay. Regulatory processes appear to be specifically localized: in particular, differential growth occurs where the elongation rate drops. Finally, impairing the graviception of the leaf on a clinostat led to reduced hook curvature but not to its loss. Altogether, our results suggest a role for proprioception in the regulation of the leaf hook shape, likely mediated via mechanical strain.

The R2R3-MYB transcription factor GhMYB1a regulates flavonol and anthocyanin accumulation in Gerbera hybrida.

Anthocyanins and flavonols have vital roles in flower coloration, plant development, and defense. Because anthocyanins and flavonols share the same subcellular localization and common biosynthetic substrates, these pathways may compete for substrates. However, the mechanism regulating this potential competition remains unclear. Here, we identified GhMYB1a, an R2R3-MYB transcription factor involved in the regulation of anthocyanin and flavonol accumulation in gerbera (Gerberahybrida). GhMYB1a shares high sequence similarity with that of other characterized regulators of flavonol biosynthesis. In addition, GhMYB1a is also phylogenetically grouped with these proteins. The overexpression of GhMYB1a in gerbera and tobacco (Nicotianatabacum) resulted in decreased anthocyanin accumulation and increased accumulation of flavonols by upregulating the structural genes involved in flavonol biosynthesis. We further found that GhMYB1a functions as a homodimer instead of interacting with basic helix-loop-helix cofactors. These results suggest that GhMYB1a is involved in regulating the anthocyanin and flavonol metabolic pathways through precise regulation of gene expression. The functional characterization of GhMYB1a provides insight into the biosynthesis and regulation of flavonols and anthocyanins.

Dimorphic Leaf Development of the Aquatic Plant Callitriche palustris L. Through Differential Cell Division and Expansion.

Heterophylly, or phenotypic plasticity in leaf form, is a remarkable feature of amphibious plants. When the shoots of these plants grow underwater, they often develop surprisingly different leaves from those that emerge in air. Among aquatic plants, it is typical for two or more distinct leaf development processes to be observed in the same individual exposed to different environments. Here, we analyze the developmental processes of heterophylly in the amphibious plant Callitriche palustris L. (Plantaginaceae). First, we reliably cultured this species under laboratory conditions and established a laboratory strain. We also established a framework for molecular-based developmental analyses, such as whole-mount in situ hybridization. We observed several developmental features of aerial and submerged leaves, including changes in form, stomata and vein formation, and transition of the meristematic zone. Then we defined developmental stages for C. palustris leaves. We found that in early stages, aerial and submerged leaf primordia had similar forms, but became discriminable through cell divisions with differential direction, and later became highly distinct via extensive cell elongation in submerged leaf primordia.

The importance of being edgy: cell geometric edges as an emerging polar domain in plant cells.

Polarity is an essential feature of multicellular organisms and underpins growth and development as well as physiological functions. In polyhedral plant cells, polar domains at different faces have been studied in detail. In recent years, cell edges (where two faces meet) have emerged as discrete spatial domains with distinct biochemical identities. Here, we review and discuss recent advances in our understanding of cell edges as functional polar domains in plant cells and other organisms, highlighting conceptual parallels and open questions regarding edge polarity.

Suppression of soft spots and excited modes in the shape deformation model with spatio-temporal growth noise.

The shapes of plant organs such as sepals are precise and reproducible, although the cells composing these organs are highly heterogeneous. We investigate the collective behavior of a shape deformation model with spatio-temporal fluctuations in elasticity (Hong et al., Dev. Cell, 38, 15, 2016). It is shown that the spatio-temporal growth noise has two opposing effect: the temporal noise promotes the reproducibility of the organ shape, whereas the spatial noise disturbs it, leading to the organ undergoing an abnormal shape deformation. To understand how such abnormality can emerge, we study the eigenvectors of the correlation matrix of the growth velocity. It is revealed that the anomalous shape deformations can be created by two independent factors: (1) excited modes where the orientations of the eigenvectors with m ≥ 2 are spatially correlated, and/or (2) soft spots where spot structures with high fluctuations in the magnitudes of the eigenvectors appear non-uniformly.

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

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.

Las agallas se definen como modificaciones del diseño y desarrollo normal de las plantas debido a una reacción específica a la presencia y actividad de un organismo foráneo. Aunque diferentes grupos de organismos tienen la habilidad de inducir agallas en plantas, las agallas inducidas por insectos son las más elaboradas y diversas. Algunas hipótesis han sido propuestas para explicar el mecanismo de inducción de las agallas de insectos. La hipótesis más general sugiere que la formación de las agallas es disparada por la acción de sustancias químicas secretadas por el insecto inductor, incluyendo reguladores de plantas como auxinas, citoquininas, ácido-3-indolacético (AIA) o bien otros tipos de compuestos. No obstante, el modo de acción de estas sustancias químicas y el mecanismo general por medio del cual el insecto podría controlar y manipular el desarrollo y fisiología de la planta es aún desconocido. Más aún, como resultado de la complejidad del proceso de inducción y desarrollo de las agallas de plantas inducidas por insectos, la hipótesis química es una explicación insuficiente e incompleta en relación con el mecanismo de inducción y morfogénesis de estas estructuras. Previas y nuevas evidencias relacionadas con el sistema de agallas de insectos, con énfasis en el proceso de inducción, fueron analizadas desde un punto de vista integral del autor para proponer en este artículo una perspectiva diferente sobre la inducción de este tipo de estructuras. Debido a la extraordinaria diversidad de formas, colores y estructuras complejas presentes en las agallas de insectos, las mismas constituyen modelos útiles para estudiar cómo la forma y la estructura son determinadas a nivel molecular en los sistemas vegetales. Además, las agallas de plantas son un importante origen de material para el estudio y exploración de nuevas sustancias químicas de interés humano, debido a las características fisiológicas y adaptativas que presentan. Considerando el control fino del proceso de morfogénesis, regulación bioquímica y complejidad estructural de las agallas de insectos, se propone que un mecanismo de inducción mediado por la inserción de elementos genéticos exógenos dentro del genoma de las células de la planta que forman la agalla podría estar involucrado en la formación de este tipo de estructuras, vía una bacteria endosimbiótica.