Herbivore-induced jasmonic acid bursts in leaves of Nicotiana attenuata mediate short-term reductions in root growth (original) (raw)
Plant Signaling & Behavior, 2009
Ethylene plays a key role in the elongation of exploratory and root hair systems in plants, as demonstrated by pharmacological modulation of the activity of ethylene biosynthesis enzymes: ACC synthase (ACS) and ACC oxidase (ACO). Thus, treatments with high concentrations (10 μM) of aminoethoxyvinylglycine (AVG, inhibitor of ACS) and 1-aminocyclopropane carboxylic acid (ACC, ethylene precursor, ACO activator) severely decrease the elongation of the exploratory root system but induce opposite effects on the root hair system: root hair length and numbers were increased in seedlings treated with ACC, whereas they were reduced in seedlings treated with AVG. Until now, such elongation changes of root architecture had not been questioned in terms of nitrate uptake. In the march issue of Plant Physiology we report that N uptake and nitrate transporter BnNrt2.1 transcript level were markedly reduced in ACC treated seedlings, but were increased in AVG treated seedlings compared to the control. 1 Because recent studies have revealed that ethylene can also modulate stomatal opening as well as root hair cell elongation, we have examined whether pharmacological modulation of ethylene biosynthesis could affect, in an integrated manner, and at a whole-plant level, the exploratory and root hair systems, through changes of stomatal conductance and water allocation between the root and shoot.
Ethylene in Seed Germination and Early Root Development
Seed germination is a model system for the analysis of plant development. Cell elongation and differentiation processes are under the control of hormones and submitted to the influence of environmental factors. Hormones (abscisic acid, auxin, gibberellic acid, ethylene and others) interact with each other as well as with diverse components of cell metabolism. Arabidopsis is the model system for the study of developmental processes in plants and research in this species is now helped by a multiplicity of resources (massive genome sequences available, collections of mutants and lines expressing GFP, direct observation in confocal microscopy among others). The analysis of seed germination in Arabidopsis using these tools offers a unique opportunity to dissect the interaction of hormonal pathways during development and its relationship to cellular processes. Ethylene is one of the hormones whose mechanism of action has been most thoroughly investigated and may serve a pivotal role in this analysis. An important requirement is the accurate description of phenotypes for the known mutants with altered sensitivity or response to hormones. This chapter reviews our recent description of root apex curvature as a new phenotype associated with the ethylene signaltransduction pathway mutants. New Arabidopsis sequences induced during germination have been recently isolated. Their expression analysis may be a useful tool to investigate hormonal interactions during seed germination. Cervantes E, De Diego JG, Gómez MD, De Las Rivas J, Igual JM, Velázquez E, Grappin P, Cercós M, Carbonell J (2001) Expression of a cysteine proteinase in chickpea (Cicer arietinum L.) is localized to provascular cells in the developing root. Journal of Plant Physiology 158, 1463-1469 Cervantes E, Tocino A (2005) Geometric analysis of Arabidopsis root apex reveals a new aspect of the ethylene signal transduction pathway in development. Journal of Plant Physiology 162, 1038-1045 Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15, 545-559 Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262, 539-544 Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. Journal of Biological Chemistry 277, 19861-19866 Chiwocha SD, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross AR, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant Journal 42, 35-48 Clark KL, Larsen PB, Wang X, Chang C (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445 de Diego JG, Rodríguez FD, Cervantes E (2002) The control of germination in model plants: Ethylene, cell elongation and cell división cycle. In: Vendrell M (ed) Biology and Biotechnology of the Plant Hormone Ethylene III., IOS Press, pp 246-247 de Diego JG, Rodríguez FD, Rodríguez-Lorenzo JL, Grappin P, Cervantes E (2005) cDNA-AFLP analysis of seed germination in Arabidopsis thaliana identifies transposons and new genomic sequences. Journal of Plant Physiology In press Doerner P, Jorgensen J-E, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380, 520-523 Ecker JR (2004) Reentry of the Ethylene MPK6 Module. The Plant Cell 16, 3169-3173 Esashi Y (1991) Ethylene and seed germination. In: Mattoo AK, Suttle JC (eds) The Plant Hormone Ethylene, CRC Press, Boca Raton, pp 133-157 Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic Acid signaling in seeds and seedlings. Plant Cell 14S, 15-45 Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446 Garcia RL, Arza PL, Almarza FI (2001) Influence of a stationary magnetic field on water relations in lettuce seeds. Part II: Experimental results. Bioelectromagnetics 22, 596-602 Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2002) Regulation of abscisic acid signaling by the ethylene response pathway in arabidopsis. The Plant M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes and Development 13, 1678-1691 Grichko VP, Glick BR (2001) Ethylene and flooding stress in plants. Plant Physiology and Biochemistry 39, 1-9 Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115, 667-677 Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523 D'Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S, Verplancke C, Capoen W, Holsters M (2003) Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology 112, 463-572 Hirasawa E (1988) Amine oxidase in cotyledons of Pisum sativum develops as a result of the supply of oxygen through the embryonic axis during germination. Plant Physiology 88, 441-443 Hua J, Meyerowitz EM (1998) Ethylene responses are regulated by a receptor gene family in Arabidopsis thaliana. Cell 94, 261-271 Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker A, Ecker B, Meyerowitz EM (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10, 1321-1332 Huang Y, Li H, Hutchison CE, Laskey J, Kieber JJ (2003) Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant Journal 33, 221-233 Ip YT, Davis RJ (1998) Signal tansduction by the c-Jun NH2-terminal kinase (JNK)-from inflammation to development. Current Opinion in Cell Biology 10, 205-219 Iuchi S, Lin ECC (1993) Adaptation of Escherichia coli to redox environments by regulation of gene expression. Cell 66, 5-7 Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochemical Pharmacology 57, 231-245 Jackson MB (1985) Ethylene and responses of plants to soil waterlogging and submergence. Annual Review of Plant Physiology 36, 145-174 Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126, 1055-1060 Kakimoto T (1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982-985 Kende H (2001) Hormone response mutants. A plethora of surprises. Plant Physiology 125, 81-84 Kende H, van der Knaap E, Cho H-T (1998) Deepwater rice: A model plant to study stem elongation. Plant Physiology 118, 1105-1110 Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446-451 Kieber JJ, Rothenberg M, Roman G, Feldman KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72, 427-441 Le J, Vandenbussche GF, Van der Straaten D, Verbelen JP (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up-and down-regulated and uncoupled from differentiation. Plant Physiology 125, 519-522 Le J, Vandenbussche GF, Van der Straaten D, Verbelen JP (2004) Position and cell type-dependent microtubule reorientation characterizes the early response of the Arabidopsis root epidermis to ethylene. Physiologia Plantarum 121, 513-522 Leprince O, Hoekstra FA (1998) The responses of cytochrome redox state and energy metabolism to dehydration support a role for cytoplasmic viscosity in desiccation tolerance. (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regulation 46, 45-51 Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2·-, H2O2, and ·OH) by maize roots and their role in wall loosening and elongation growth. Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8, 1505-1517 Matilla A, Gallardo M, Puga-Hermida MI (2005) Structural, physiological and molecular aspects of heterogeneity in seeds: A review. Seed Science Research 15, 63-76 Matsushika A, Mizuno T (1998) A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain in Escherichia coli. Journal of Bacteriology 180, 3973-3977 Mayuri BG, Das TK, Tyagi JS (2002) Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR-DevS twocomponent system, Rv3134c and chaperone alpha-crystallin homologues. FEMS Microbiology Letters 211, 231-237 McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120-1130 Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214, 775-782 Mereschkovsky KS (1926) Symbiogenesis and the Origin of Species Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant...
Root growth dynamics of Nicotiana attenuata seedlings are affected by simulated herbivore attack
Plant, Cell & Environment, 2007
Many studies demonstrate resource-based trade-offs between growth and defence on a large timescale. Yet, the short-term dynamics of this growth reaction are still completely unclear, making it difficult to explain growth-defence trade-offs mechanistically. In this study, image-based non-destructive methods were used to quantify root growth reactions happening within hours following simulated herbivore attack. The induction of wound reactions in Nicotiana attenuata in the seedling stage led to transiently decreased root growth rates. Application of the oral secretion of the specialist herbivore Manduca sexta to the leaves led to a transient decrease in root growth that was more pronounced than if a mere mechanical wounding was imposed. Root growth reduction was more pronounced than leaf growth reduction. When fatty acid-amino acid conjugates (FACs) were applied to wounds, root growth reduction occurred in the same intensity as when oral secretion was applied. Timing of the transient growth reduction coincided with endogenous bursts of jasmonate (JA) and ethylene emissions reported in literature. Simulation of a wound response by applying methyl jasmonate (MeJA) led to more prolonged negative effects on root growth. Increased nicotine concentrations, trichome lengths and densities were observed within 72 h in seedlings that were treated with MeJA or that were mechanically wounded. Overall, these reactions indicate that even in a very early developmental stage, the diversion of plant metabolism from primary (growth-sustaining) to secondary (defence-related) metabolism can cause profound alterations of plant growth performance.
PLANT PHYSIOLOGY, 2010
Jasmonic acid (JA) and ethylene (ET) are known to play important roles in mediating plant defense against herbivores, but how they affect development in herbivore-attacked plants is unknown. We used JA-deficient (silenced in LIPOXYGENASE3 [asLOX3]) and ET-insensitive (expressing a mutated dominant negative form of ETHYLENE RESPONSE1 [mETR1]) Nicotiana attenuata plants, and their genetic cross (mETR1asLOX3), to examine growth and development of these plants under simulated herbivory conditions. At the whole plant level, both hormones suppressed leaf expansion after the plants had been wounded and the wounds had been immediately treated with Manduca sexta oral secretions (OS). In addition, ectopic cell expansion was observed around both water-and OS-treated wounds in mETR1asLOX3 leaves but not in mETR1, asLOX3, or wild-type leaves. Pretreating asLOX3 leaves with the ET receptor antagonist 1-methylcyclopropane resulted in local cell expansion that closely mimicked the mETR1asLOX3 phenotype. We found higher auxin (indole-3-acetic acid) levels in the elicited leaves of mETR1asLOX3 plants, a trait that is putatively associated with enhanced cell expansion and leaf growth in this genotype. Transcript profiling of OS-elicited mETR1asLOX3 leaves revealed a preferential accumulation of transcripts known to function in cell wall remodeling, suggesting that both JA and ET act as negative regulators of these genes. We propose that in N. attenuata, JA-ET cross talk restrains local cell expansion and growth after herbivore attack, allowing more resources to be allocated to induced defenses against herbivores.
Root Formation in Ethylene-Insensitive Plants1
1999
Experiments with ethylene-insensitive tomato (Lycopersicon esculentum) and petunia (Petunia ؋ hybrida) plants were conducted to determine if normal or adventitious root formation is affected by ethylene insensitivity. Ethylene-insensitive Never ripe (NR) tomato plants produced more belowground root mass but fewer aboveground adventitious roots than wild-type Pearson plants. Applied auxin (indole-3-butyric acid) increased adventitious root formation on vegetative stem cuttings of wild-type plants but had little or no effect on rooting of NR plants. Reduced adventitious root formation was also observed in ethylene-insensitive transgenic petunia plants. Applied 1-aminocyclopropane-1-carboxylic acid increased adventitious root formation on vegetative stem cuttings from NR and wild-type plants, but NR cuttings produced fewer adventitious roots than wild-type cuttings. These data suggest that the promotive effect of auxin on adventitious rooting is influenced by ethylene responsiveness. Seedling root growth of tomato in response to mechanical impedance was also influenced by ethylene sensitivity. Ninety-six percent of wild-type seedlings germinated and grown on sand for 7 d grew normal roots into the medium, whereas 47% of NR seedlings displayed elongated taproots, shortened hypocotyls, and did not penetrate the medium. These data indicate that ethylene has a critical role in various responses of roots to environmental stimuli.
Root Formation in Ethylene-Insensitive Plants
PLANT PHYSIOLOGY, 1999
Experiments with ethylene-insensitive tomato (Lycopersicon esculentum) and petunia (Petunia ؋ hybrida) plants were conducted to determine if normal or adventitious root formation is affected by ethylene insensitivity. Ethylene-insensitive Never ripe (NR) tomato plants produced more belowground root mass but fewer aboveground adventitious roots than wild-type Pearson plants. Applied auxin (indole-3-butyric acid) increased adventitious root formation on vegetative stem cuttings of wild-type plants but had little or no effect on rooting of NR plants. Reduced adventitious root formation was also observed in ethylene-insensitive transgenic petunia plants. Applied 1-aminocyclopropane-1-carboxylic acid increased adventitious root formation on vegetative stem cuttings from NR and wild-type plants, but NR cuttings produced fewer adventitious roots than wild-type cuttings. These data suggest that the promotive effect of auxin on adventitious rooting is influenced by ethylene responsiveness. Seedling root growth of tomato in response to mechanical impedance was also influenced by ethylene sensitivity. Ninety-six percent of wild-type seedlings germinated and grown on sand for 7 d grew normal roots into the medium, whereas 47% of NR seedlings displayed elongated taproots, shortened hypocotyls, and did not penetrate the medium. These data indicate that ethylene has a critical role in various responses of roots to environmental stimuli.
Modulation of Plant Defenses by Ethylene
Journal of Plant Growth Regulation, 2007
Ethylene (ET) plays a critical role in the activation of plant defenses against different biotic stresses through its participation in a complex signaling network that includes jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). Pathogen attack, wounding, and herbivory trigger asymmetric activation of this defense signaling network, thereby affecting the final balance of interactions between its components and establishing a targeted response to the initial threat. Ethylene’s contribution to the modulation of this defense network relies on the complexity of the regulation of multigene families involved in ET biosynthesis, signal transduction, and crosstalk and enables the plant to fine-tune its response. The function of the members of these multigene families is tightly regulated at transcriptional, post-transcriptional, and post-translational levels. It is generally accepted that ET cooperates with JA in the activation of defenses against necrotrophic pathogens and antagonizes SA-dependent resistance against biotrophic pathogens. However, this is likely an oversimplified view, because cooperative interactions between ET and SA pathways have been reported and ET has been implicated in the activation of defenses against some biotrophic and hemibiotrophic pathogens. Therefore, deciphering ET’s place in this hormonal network is essential to understanding how the cell orchestrates an optimal response to a specific biotic stress.
Involvement of ethylene in the rooting of seedling shoot cultures of Bixa orellana L
In Vitro Cellular & Developmental Biology - Plant, 2009
Using seedlings derived from the shoot apex of annatto (Bixa orellana L. cv. Bico-de-Pato) we observed the rooting frequency of B. orellana, the number and length of roots and the rate of ethylene production during 30 d in culture. The rhizogenesis response was affected by auxins (NAA or IBA) and by both the ethylene biosynthesis precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and the inhibitor 2-aminoethoxyvinylglycine (AVG). Auxin supplementation to the medium resulted in root induction, ethylene production, and an undesirable callusing in the epidermal and cortical tissues. Irrespective of the presence of auxins, supplementing the medium with ACC promoted ethylene biosynthesis and callusing, which resulted in increased cell proliferation mainly in the cortical and vascular tissues, while the epidermis was mostly unaltered. In both ACC and auxin-supplemented medium, increased ethylene production and callusing occurred, suggesting a synergistic effect between these two responses. ACC was capable of inducing adventitious root formation, but the roots produced had a wrinkled appearance when compared to normal roots. Conversely, AVG reduced ethylene production and callusing, while the epidermis, cortex, and inner tissues remained unaltered, regardless of the presence of auxins. AVG was beneficial in these aspects, although its application led to a reduction in the number of roots and in the average root length. In conclusion, it was not possible to establish a direct relation between ethylene and rooting, but we hypothesize that, under the experimental conditions described, ethylene may enhance tissue sensitivity to auxin. However, ethylene did not seem essential to the rhizogenesis process in annatto.
Ethylene as an endogenous inhibitor of root regeneration in tomato leaf discs cultured in vitro
Physiologia …, 1980
We examined ethylene effects on root regeneration in tomato leaf discs cultured in vitro. Applied ethylene or Ethephon did not stimulate rooting in the leaf discs. In the presence of indoleacetic acid, 5 X 10^ M, these substances significantly inhibited root formation, Ethylene production (nl C2H4 • (24 h)~^ • flask"') was positively correlated with increased IAA concentrations at various times during the culture period and, as a consequence, with the rooting response after 168 h. However, separate testing of equimolar concentrations of seven different auxins and auxin-like compounds showed no positive correlation between the rate of ethylene production and subsequent rooting response. Aeration of gas-tight flasks containing leaf discs and absorption of ethylene evolved from the discs by mercuric perchlorate in gas-tight flasks or pre-treatment of leaf discs with AgNO3 significantly enhanced IAA induced root regeneration. Thus, these studies indicate that ethylene is not a rooting hormone per se. Furthermore, ethylene (whether applied externally or synthesized by the tissue) does not appear to account for the ability of auxin to stimulate rooting.
Cross-regulation of Arabidopsis root growth by plant hormones auxins and ethylene
Biological Communications
We investigated the cross-talk between auxin (IAA) and ethylene in the control of root growth of Arabidopsis plants (Arabidopsis thaliana). The root growth of ethylene insensitive etr1-1 and auxin insensitive tir1 mutants under the effect of IAA and 1-methylcyclopropene (1-MCP, inhibitor of ethylene perception) was compared, respectively, with that of the wild type ecotype Columbia (Col-0). Roots of Col-0 were shorter than those of the etr1-1 mutant. The addition of IAA (5.7 × 10-6 М) to the growth medium led to 20 % root shortening in Col-0 plants, but not in etr1-1 mutants. Thus, the capacity of plants for ethylene perception contributes to the control of root length and its sensitivity to IAA. Roots of etr1-1 were less heavy than in Col-0, indicating that ethylene maintains root mass accumulation. Treatment with IAA caused a decrease in root mass of both genotypes (resulting in a 25 and 10 % decline in the root mass of Col-0 and etr1-1 as compared to the corresponding control), suggesting that IAA may influence root biomass accumulation independently of ethylene. However, sensitivity to ethylene increases plant responsiveness to IAA. Mutation in the auxin receptor decreased the sensitivity of roots to inactivation of ethylene receptors: treatment with 1-MCP resulted in a 40 % decline in the root mass of Col-0 and only a 10 % decrease in tir1. The decrement in sensitivity to auxins in the tir1 mutant decreased the responsiveness of root biomass to 1-MCP-treatment. These data suggest an additive action of ethylene and auxins on accumulation of root biomass.