The inter‐kingdom volatile signal indole promotes root development by interfering with auxin signalling

Recently, emission of volatile organic compounds (VOCs) has emerged as a mode of communication between bacteria and plants. Although some bacterial VOCs that promote plant growth have been identified, their underlying mechanism of action is unknown. Here we demonstrate that indole, which was identified using a screen for Arabidopsis growth promotion by VOCs from soil‐borne bacteria, is a potent plant‐growth modulator. Its prominent role in increasing the plant secondary root network is mediated by interfering with the auxin‐signalling machinery. Using auxin reporter lines and classic auxin physiological and transport assays we show that the indole signal invades the plant body, reaches zones of auxin activity and acts in a polar auxin transport‐dependent bimodal mechanism to trigger differential cellular auxin responses. Our results suggest that indole, beyond its importance as a bacterial signal molecule, can serve as a remote messenger to manipulate plant growth and development.     

Flavonoids act as negative regulators of auxin transport in vivo in arabidopsis

Polar transport of the plant hormone auxin controls many aspects of plant growth and development. A number of synthetic compounds have been shown to block the process of auxin transport by inhibition of the auxin efflux carrier complex. These synthetic auxin transport inhibitors may act by mimicking endogenous molecules. Flavonoids, a class of secondary plant metabolic compounds, have been suggested to be auxin transport inhibitors based on their in vitro activity. The hypothesis that flavonoids regulate auxin transport in vivo was tested in Arabidopsis by comparing wild-type (WT) and transparent testa (tt4) plants with a mutation in the gene encoding the first enzyme in flavonoid biosynthesis, chalcone synthase. In a comparison between tt4 and WT plants, phenotypic differences were observed, including three times as many secondary inflorescence stems, reduced plant height, decreased stem diameter, and increased secondary root development. Growth of WT Arabidopsis plants on naringenin, a biosynthetic precursor to those flavonoids with auxin transport inhibitor activity in vitro, leads to a reduction in root growth and gravitropism, similar to the effects of synthetic auxin transport inhibitors. Analyses of auxin transport in the inflorescence and hypocotyl of independent tt4 alleles indicate that auxin transport is elevated in plants with a tt4 mutation. In hypocotyls of tt4, this elevated transport is reversed when flavonoids are synthesized by growth of plants on the flavonoid precursor, naringenin. These results are consistent with a role for flavonoids as endogenous regulators of auxin transport.     

The Relationship of Indole-3-Acetic Acid Content and Growth of Crown-Gall Tumor Tissues of Tobacco in Culture

We have measured the content of the auxin, indole-3-acetic acid (IAA), in a cloned, crown-gall teratoma line of Nicotiana tabacum L. cv. 'Turkish' by a highly specific and sensitive radioimmunoassay. This tissue line, which does not require auxin for continuous growth in culture, exhibits two phases of growth. During the first phase, which lasts about two weeks after subculturing, growth is exponential on a fresh weight basis and the content of IAA is about 10⁻⁷–10⁻⁶ mol. kg⁻¹, but variable. During the second phase, growth rate declines gradually and the IAA content of the tissue drops dramatically; however, this drop does not result from a net loss of auxin by the tissue. The rate of growth during the exponential phase was not correlated with the IAA content of the tissue, but was strongly correlated with the IAA content of the inoculum. We found that rapidly growing leaves of Turkish tobacco have roughly the same IAA content as cultured teratoma tissues. Moreover, both tissues exhibited a similar relationship between auxin content expressed per leaf or per tissue explant and growth. These findings do not support the hypothesis that the autonomous growth of plant tumors results from an abnormally high content of auxin in the tissue.     

The shade avoidance syndrome: A non-Markovian stochastic growth model

Plants at high population density compete for light, showing a series of physiological responses known as the shade avoidance syndrome. These responses are controlled by the synthesis of the hormone auxin, which is regulated by two signals, an environmental one and an internal one. Considering that the auxin signal induces plant growth after a time lag, this work shows that plant growth can be modelled in terms of an energy-like function extremization, provided that the Markov property is not applied. The simulated height distributions are bimodal and right skewed, as in real community of plants. In the case of isolated plants, theoretical growth dynamics and speed correctly fit Arabidopsis thaliana experimental data reported in literature. Moreover, the growth dynamics of this model is shown to be consistent with the biomass production function of an independent model. These results suggest that memory effects play a non-negligible role in plant growth processes.     

Effect of simulated microgravity on auxin polar transport in inflorescence axis of Arabidopsis thaliana.

The morphology, growth and development of higher plants are strongly influenced by environmental stimuli on the earth, which affect the changes in the dynamics of plant hormones in plants. Qualitative and quantitative changes in plant hormones are the most important internal factor to regulate plant growth and development. Among them, auxin (IAA) is of most significant. There are numerous reports concerning the physiological roles of auxin in plant growth and development (Matthysse and Scott 1984). One of the characteristics of auxin is to have the ability of polar transport along the vector of gravity on the earth (Schneider and Wightman 1978), suggesting that the activity of auxin polar transport is also important for the growth and development of plants. It has recently been reported that the normal activity of auxin polar transport in inflorescence axis of Arabidopsis thaliana was required for flower formation (Okada et al. 1991, Ueda et al. 1992). Considering the above evidence together with the fact that gravity affects the morphology, growth and development of higher plants, gravity might affect the qualitative and quantitative changes in plant hormones including the activity of auxin polar transport. In this paper, we report the effect of microgravity condition simulated by a three-dimensional (3-D) or a horizontal clinostat on the activity of auxin polar transport in inflorescence axis of Arabidopsis thaliana.     

Channelling auxin action: modulation of ion transport by indole-3-acetic acid

The growth hormone auxin is a key regulator of plant cell division and elongation. Since plants lack muscles, processes involved in growth and movements rely on turgor formation, and thus on the transport of solutes and water. Modern electrophysiological techniques and molecular genetics have shed new light on the regulation of plant ion transporters in response to auxin. Guard cells, hypocotyls and coleoptiles have advanced to major model systems in studying auxin action. This review will therefore focus on the molecular mechanism by which auxin modulates ion transport and cell expansion in these model cell types.     

Plant signalling: the inexorable rise of auxin

The flow of signalling molecules across a field of cells to generate a pattern that is then transduced into a differential response in those cells is a fundamental concept in developmental biology. Recent studies have identified a system that regulates the flux of the growth factor auxin through plant tissues via the subcellular asymmetric localization of specific transporters. The recurrent use of this auxin transport system in different developmental and physiological contexts reveals a fundamental mechanism underpinning organogenesis, stem cell positioning and the growth response of the plant to the environment. Here, I will discuss key advances in the identification of auxin transporters and their integration with auxin signal transduction pathways.     

A molecular basis for auxin action.

The plant hormone auxin is central in the regulation of growth and development, however, the molecular basis for its action has remained enigmatic. In the absence of a molecular model, the wide range of responses elicited by auxin have been difficult to explain. Recent advances using molecular genetic approaches in Arabidopsis have led to the isolation of a number of key genes involved in auxin action. Of particular importance are genes involved in channelling polar auxin transport through the plant. In addition a model for auxin signal transduction, centred on regulated protein degradation, has been developed.     

The hormonal regulation of axillary bud growth in Arabidopsis

Apically derived auxin has long been known to inhibit lateral bud growth, but since it appears not to enter the bud, it has been proposed that its inhibitory effect is mediated by a second messenger. Candidates include the plant hormones ethylene, cytokinin and abscisic acid. We have developed a new assay to study this phenomenon using the model plant Arabidopsis. The assay allows study of the effects of both apical and basal hormone applications on the growth of buds on excised nodal sections. We have shown that apical auxin can inhibit the growth of small buds, but larger buds were found to have lost competence to respond. We have used the assay with nodes from wild-type and hormone-signalling mutants to test the role of ethylene, cytokinin and abscisic acid in bud inhibition by apical auxin. Our data eliminate ethylene as a second messenger for auxin-mediated bud inhibition. Similarly, abscisic acid signalling is not to be required for auxin action, although basally applied abscisic can enhance inhibition by apical auxin and apically applied abscisic acid can reduce it. By contrast, basally applied cytokinin was found to release lateral buds from inhibition by apical auxin, while apically applied cytokinin dramatically increased the duration of inhibition. These results are consistent with cytokinin acting independently to regulate bud growth, rather than as a second messenger for auxin. However, in the absence of cytokinin-signalling mutants, a role for cytokinin as a second messenger for auxin cannot be ruled out.     

Plant growth hormones suppress the development of Harpophora maydis,the cause of late wilt in maize

Late wilt, a severe vascular disease of maize caused by the fungus Harpophora maydis, is characterized by rapid wilting of maize plants before tasseling and until shortly before maturity. The pathogen is currently controlled by resistant maize cultivars, but the disease is constantly spreading to new areas. The plant’s late phenological stage at which the disease appears suggests that plant hormones may be involved in the pathogenesis. This work revealed that plant growth hormones, auxin (Indole-3-acetic acid) and cytokinin (kinetin), suppress H. maydis in culture media and in a detached root assay. Kinetin, and even more auxin, caused significant suppression of fungus spore germination. Gibberellic acid did not alter colony growth rate but had a signal suppressive effect on the pathogens’ spore germination. In comparison, ethylene and jasmonic acid, plant senescing and defense response regulators, had minor effects on colony growth and spore germination rate. Their associate hormone, salicylic acid, had a moderate suppressive effect on spore germination and colony growth rate, and a strong influence when combined with auxin. Despite the anti-fungal auxin success in vitro, field experiments with dimethylamine salt of  2,4-dichlorophenoxyacetic acid (that mimics the influence of auxin) failed to suppress the late wilt. The lines of evidence presented here reveal the suppressive influence of the three growth hormones studied on fungal development and are important to encourage further and more in-depth examinations of this intriguing hormonal complex regulatory and its role in the maize-H. maydis interactions.     

Regulating the regulator: the control of auxin transport

With the discovery of the phytohormone auxin in the late 1920s, it became possible to link the regulation of complex plant growth responses to a single biologically active compound. Among all the plant growth regulators characterised so far, only auxin appears to be actively transported throughout the plant to create complex variations in concentration patterns and flow directions over time. This stimulated interest in the specific mechanisms underlying auxin transport as key factors in plant growth responses. Research in the last decade revealed several genes involved in the controlled transport of auxin and greatly improved our understanding of the basic principles of auxin-mediated responses. We are at this point, however, only starting to understand the complex interplay and control of factors that ultimately underlie the observed spatiotemporal variations in auxin transport and thus mediate plant growth and environmental responses. This review highlights important findings that provide us with a framework of molecular players and potential regulatory mechanisms that should contribute to the formulation of a comprehensive dynamic model of spatiotemporal auxin distribution.     

Modelling of auxin transport affected by gravity and differential radial growth

When a tree stem deviates from verticality, as a result of different environmental factors, patterns of differential radial growth appear. Higher rates of wood production have been observed on the lower side of the tree and lower rates in the opposite side. Biological studies on plant hormones have shown that the concentration of auxin induces radial growth. They also have demonstrated the redistribution of auxin transport in response to gravity. Auxin is then designated as a mediator for differential growth. This paper presents a model for three-dimensional (3-D) auxin transport in conifer trees, which includes gravity dependence. We obtain realistic heterogeneous patterns of auxin distribution over the tree. Then, we propose a law of growth based on auxin concentration to simulate successive differential radial growths. The predicted growths are compared with experimental results of reconstruction of 3-D annual growth of Radiata pine.     

Dynamic integration of auxin transport and signalling

Recent years have seen rapid progress in our understanding of the mechanism of action of the plant hormone auxin. A major emerging theme is the central importance of the interplay between auxin signalling and the active transport of auxin through the plant to create dynamic patterns of auxin accumulation. Even in tissues where auxin distribution patterns appear stable, they are the product of standing waves, with auxin flowing through the tissue, maintaining local pockets of high and low concentration. The auxin distribution patterns result in changes in gene expression to trigger diverse, context-dependent growth and differentiation responses. Multi-level feedback loops between the signal transduction network and the auxin transport network provide self-stabilising patterns that remain sensitive to the external environment and to the developmental progression of the plant. The full biological implications of the behaviour of this system are only just beginning to be understood through a combination of experimental manipulation and mathematical modelling.     

4-Chloroindole-3-acetic acid and plant growth

4-Chloroindole-3-acetic acid (4-Cl-IAA) is a potent auxin in various auxin bioassays. Researchers have used 4-Cl-IAA as well as other halogenated auxins in biological assays to understand the structural features of auxins required to induce auxin mediated growth in plants. 4-Cl-IAA is a naturally occurring auxin in plants from the Vicieae tribe of the Fabaceae family; and 4-Cl-IAA has also been identified in one species outside the Vicieae tribe, Pinus sylvestris. The apparent function of the unique auxin 4-Cl-IAA in normal plant growth and development will be discussed with a focus on Pisum sativum and Vicia faba     

生长素合成途径的研究进展

生长素是一类含有一个不饱和芳香族环和一个乙酸侧链的内源激素, 参与植物生长发育的许多过程。植物和一些侵染植物的病原微生物都可以通过改变生长素的合成来调节植株的生长。吲哚-3-乙酸(IAA)是天然植物生长素的主要活性成分。近年来, 随着IAA生物合成过程中一些关键调控基因的克隆和功能分析, 人们对IAA的生物合成途径有了更加深入的认识。IAA的生物合成有依赖色氨酸和非依赖色氨酸两条途径。依据IAA合成的中间产物不同, 依赖色氨酸的生物合成过程通常又划分成4条支路: 吲哚乙醛肟途径、吲哚丙酮酸途径、色胺途径和吲哚乙酰胺途径。该文综述了近几年在IAA生物合成方面取得的新进展。     

Auxin in action: signalling, transport and the control of plant growth and development

Hormones have been at the centre of plant physiology research for more than a century. Research into plant hormones (phytohormones) has at times been considered as a rather vague subject, but the systematic application of genetic and molecular techniques has led to key insights that have revitalized the field. In this review, we will focus on the plant hormone auxin and its action. We will highlight recent mutagenesis and molecular studies, which have delineated the pathways of auxin transport, perception and signal transduction, and which together define the roles of auxin in controlling growth and patterning.     

Effect of potato seed-tuber age on plant establishment and amelioration of age-linked effects with auxin

Studies were conducted to characterize the effect of advanced potato (Solanum tuberosum L.) seed-tuber age on plant growth potential and whole-plant morphology. Plant growth from single-eye seedcores from 5- to 18-month old `Russet Burbank' seedtubers was compared. Loss in apical dominance was apparent with advanced age. On a per-core basis, the amount of plant dry weight was equal for the two ages at 30 days from planting. However, individual plants from older cores displayed reduced shoot, root and leaf dry weights, leaf area, and leaf number. These effects reflected altered dry-matter partitioning and contributed to an overall change in plant morphology with advanced age. On a total seedcore basis, relative growth rate of plants from older seedcores was greater than that from younger seedcores over the 30 day growth interval. Leaf area ratio was also greater for plants from the older seedcores; however, unit leaf rate was not affected by tuber age and plants from both young and old seedcores assimilated dry matter at the same rate. Age-induced differences in growth indices reflected differences in the degree of plant differentiation over the interval of study. Treating younger seedcores with 1-naphthaleneacetic acid (NAA) prior to planting inhibited overall plant growth. In older cores, NAA stimulated root growth, restored apical dominance, decreased leaf number per plant, and increased average leaf area per leaf. In short, NAA altered the morphology of plants growing from older seedcores to more closely resemble that of plants growing from younger seedcores. While auxin significantly altered plant form, vigor of plants from older seedcores was not fully restored by auxin treatment, indicating that age-reduced vigor of potato seed-tubers is not solely mediated by auxin.     

The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling

The rate and plane of cell division and anisotropic cell growth are critical for plant development and are regulated by diverse mechanisms involving several hormone signaling pathways. Little is known about peptide signaling in plant growth; however, Arabidopsis thaliana POLARIS (PLS), encoding a 36-amino acid peptide, is required for correct root growth and vascular development. Mutational analysis implicates a role for the peptide in hormone responses, but the basis of PLS action is obscure. Using the Arabidopsis root as a model to study PLS action in plant development, we discovered a link between PLS, ethylene signaling, auxin homeostasis, and microtubule cytoskeleton dynamics. Mutation of PLS results in an enhanced ethylene-response phenotype, defective auxin transport and homeostasis, and altered microtubule sensitivity to inhibitors. These defects, along with the short-root phenotype, are suppressed by genetic and pharmacological inhibition of ethylene action. PLS expression is repressed by ethylene and induced by auxin. Our results suggest a mechanism whereby PLS negatively regulates ethylene responses to modulate cell division and expansion via downstream effects on microtubule cytoskeleton dynamics and auxin signaling, thereby influencing root growth and lateral root development. This mechanism involves a regulatory loop of auxin-ethylene interactions.     

Tissue‐specific profiling of the Arabidopsis thaliana auxin metabolome

The plant hormone auxin is believed to influence almost every aspect of plant growth and development. Auxin transport, biosynthesis and degradation combine to form gradients of the hormone that influence a range of key developmental and environmental response processes. There is abundant genetic evidence for the existence of multiple pathways for auxin biosynthesis and degradation. The complexity of these pathways makes it difficult to obtain a clear picture of the relative importance of specific metabolic pathways during development. We have developed a sensitive mass spectrometry‐based method to simultaneously profile the majority of known auxin precursors and conjugates/catabolites in small amounts of Arabidopsis tissue. The method includes a new derivatization technique for quantification of the most labile of the auxin precursors. We validated the method by profiling the auxin metabolome in root and shoot tissues from various Arabidopsis thaliana ecotypes and auxin over‐producing mutant lines. Substantial differences were shown in metabolite patterns between the lines and tissues. We also found differences of several orders of magnitude in the abundance of auxin metabolites, potentially indicating the relative importance of these compounds in the maintenance of auxin levels and activity. The method that we have established will enable researchers to obtain a better understanding of the dynamics of auxin metabolism and activity during plant growth and development.