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1.  Hormones talking 
Plant Signaling & Behavior  2012;7(12):1698-1701.
The proper development of fruits is important for the sexual reproduction and propagation of many plant species. The fruit of Arabidopsis derives from the fertilized gynoecium, which initiates at the center of the flower and obtains its final shape, size, and functional tissues through progressive stages of development. Hormones, specially auxins, play important roles in gynoecium and fruit patterning. Cytokinins, which act as counterparts to auxins in other plant tissues, have been studied more in the context of ovule formation and parthenocarpy. We recently studied the role of cytokinins in gynoecium and fruit patterning and found that they have more than one role during gynoecium and fruit patterning. We also compared the cytokinin response localization to the auxin response localization in these organs, and studied the effects of spraying cytokinins in young flowers of an auxin response line. In this addendum, we discuss further the implications of the observed results in the knowledge about the relationship between cytokinins and auxins at the gynoecium.
PMCID: PMC3578912  PMID: 23072997
gynoecium; fruit; patterning and development; auxin; cytokinin
2.  Role of auxin-responsive genes in biotic stress responses 
Plant Signaling & Behavior  2009;4(9):846-848.
Although the phytohormone auxin has been implicated primarily in developmental processes, some recent studies suggest its involvement in stress/defense responses as well. Recently, we identified auxin-responsive genes and reported their comprehensive transcript profiling during various stages of development and abiotic stress responses in crop plant rice. The analysis revealed tissue-specific and overlapping expression profiles of auxin-responsive genes during various stages of reproductive development. In addition, a large number of auxin-responsive genes were also found to be differentially expressed under various abiotic stress conditions. Here, we further analyze the expression profiles of auxin-responsive genes during various biotic stress conditions. Several auxin-responsive genes showed response to biotic stress as well. Our analysis provides evidence for role of auxin in plant defense responses and suggests cross-talk between auxin, abiotic stress and biotic stress signaling pathways.
PMCID: PMC2802801  PMID: 19847104
auxin; auxin-responsive genes; biotic stress; rice (Oryza sativa); microarray
3.  Auxin and Monocot Development 
Monocots are known to respond differently to auxinic herbicides; hence, certain herbicides kill broadleaf (i.e., dicot) weeds while leaving lawns (i.e., monocot grasses) intact. In addition, the characters that distinguish monocots from dicots involve structures whose development is controlled by auxin. However, the molecular mechanisms controlling auxin biosynthesis, homeostasis, transport, and signal transduction appear, so far, to be conserved between monocots and dicots, although there are differences in gene copy number and expression leading to diversification in function. This article provides an update on the conservation and diversification of the roles of genes controlling auxin biosynthesis, transport, and signal transduction in root, shoot, and reproductive development in rice and maize.
Monocots and dicots share similar mechanisms for auxin biosynthesis, transport, and signaling, despite displaying big differences in the structures controlled by this phytohormone.
PMCID: PMC2829952  PMID: 20300208
4.  AUX/LAX family of auxin influx carriers—an overview 
Auxin regulates several aspects of plant growth and development. Auxin is unique among plant hormones for exhibiting polar transport. Indole-3-acetic acid (IAA), the major form of auxin in higher plants, is a weak acid and its intercellular movement is facilitated by auxin influx and efflux carriers. Polarity of auxin movement is provided by asymmetric localization of auxin carriers (mainly PIN efflux carriers). PIN-FORMED (PIN) and P-GLYCOPROTEIN (PGP) family of proteins are major auxin efflux carriers whereas AUXIN1/LIKE-AUX1 (AUX/LAX) are major auxin influx carriers. Genetic and biochemical evidence show that each member of the AUX/LAX family is a functional auxin influx carrier and mediate auxin related developmental programmes in different organs and tissues. Of the four AUX/LAX genes, AUX1 regulates root gravitropism, root hair development and leaf phyllotaxy whereas LAX2 regulates vascular development in cotyledons. Both AUX1 and LAX3 have been implicated in lateral root (LR) development as well as apical hook formation whereas both AUX1 and LAX1 and possibly LAX2 are required for leaf phyllotactic patterning.
PMCID: PMC3475149  PMID: 23087694
AUXLAX; auxin transport; auxin; AUX1; LAX1; LAX2; LAX3; influx carriers
5.  Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin 
PLoS ONE  2013;8(3):e57813.
How instructive signals are translated into robust and predictable changes in growth is a central question in developmental biology. Recently, much interest has centered on the feedback between chemical instructions and mechanical changes for pattern formation in development. In plants, the patterned arrangement of aerial organs, or phyllotaxis, is instructed by the phytohormone auxin; however, it still remains to be seen how auxin is linked, at the apex, to the biochemical and mechanical changes of the cell wall required for organ outgrowth. Here, using Atomic Force Microscopy, we demonstrate that auxin reduces tissue rigidity prior to organ outgrowth in the shoot apex of Arabidopsis thaliana, and that the de-methyl-esterification of pectin is necessary for this reduction. We further show that development of functional organs produced by pectin-mediated ectopic wall softening requires auxin signaling. Lastly, we demonstrate that coordinated localization of the auxin transport protein, PIN1, is disrupted in a naked-apex produced by increasing cell wall rigidity. Our data indicates that a feedback loop between the instructive chemical auxin and cell wall mechanics may play a crucial role in phyllotactic patterning.
PMCID: PMC3595255  PMID: 23554870
6.  Modeling Auxin-regulated Development 
The phytohormone auxin plays an essential role in many aspects of plant growth and development. Its patterning, intercellular transport, and means of signaling have been extensively studied both in experiments and computational models. Here, we present a review of models of auxin-regulated development in different plant tissues. This includes models of organ initiation in the shoot apical meristem, development of vascular strands in leafs and stems, and auxin-related functioning in roots. The examples show how mathematical modeling can help to examine expected and unexpected behavior of the system, challenge our knowledge and hypotheses, obtain quantitative results, or suggest new experiments and ways to approach a problem.
Computer simulations of plant responses to auxin explain previously perplexing aspects of the transport, regulation, and metabolism of this phytohormone.
PMCID: PMC2828283  PMID: 20182620
7.  The Arabidopsis IDD14, IDD15, and IDD16 Cooperatively Regulate Lateral Organ Morphogenesis and Gravitropism by Promoting Auxin Biosynthesis and Transport 
PLoS Genetics  2013;9(9):e1003759.
The plant hormone auxin plays a critical role in regulating various aspects of plant growth and development, and the spatial accumulation of auxin within organs, which is primarily attributable to local auxin biosynthesis and polar transport, is largely responsible for lateral organ morphogenesis and the establishment of plant architecture. Here, we show that three Arabidopsis INDETERMINATE DOMAIN (IDD) transcription factors, IDD14, IDD15, and IDD16, cooperatively regulate auxin biosynthesis and transport and thus aerial organ morphogenesis and gravitropic responses. Gain-of-function of each IDD gene in Arabidopsis results in small and transversally down-curled leaves, whereas loss-of-function of these IDD genes causes pleiotropic phenotypes in aerial organs and defects in gravitropic responses, including altered leaf shape, flower development, fertility, and plant architecture. Further analyses indicate that these IDD genes regulate spatial auxin accumulation by directly targeting YUCCA5 (YUC5), TRYPTOPHAN AMINOTRANSFERASE of ARABIDOPSIS1 (TAA1), and PIN-FORMED1 (PIN1) to promote auxin biosynthesis and transport. Moreover, mutation or ectopic expression of YUC suppresses the organ morphogenic phenotype and partially restores the gravitropic responses in gain- or loss-of-function idd mutants, respectively. Taken together, our results reveal that a subfamily of IDD transcription factors plays a critical role in the regulation of spatial auxin accumulation, thereby controlling organ morphogenesis and gravitropic responses in plants.
Author Summary
Auxin is a key plant hormone and the spatial accumulation of auxin is essential for lateral organ morphogenesis and gravitropic responses in higher plants. However, the various mechanisms through which spatial auxin accumulation is regulated remain to be fully elucidated. Here, we identify a gain-of-function mutant of Arabidopsis IDD14 that exhibits small and transversally down-curled leaves. Further characterization of both gain- and loss-of-function mutants in IDD14 and its close homologs, IDD15 and IDD16, reveals that these three IDD transcription factors function redundantly and cooperatively in the regulation of multiple aspects of lateral organ morphogenesis and gravitropic responses. We further demonstrate that these IDD transcription factors influence the spatial accumulation of auxin by directly targeting auxin biosynthetic and transport genes to activate their expression. These findings identify a subfamily of IDD transcription factors that coordinates spatial auxin gradients and thus directs lateral organ morphogenesis and gravitropic responses in plants.
PMCID: PMC3764202  PMID: 24039602
8.  Auxin at the Shoot Apical Meristem 
Plants continuously generate new tissues and organs through the activity of populations of undifferentiated stem cells, called meristems. Here, we discuss the so-called shoot apical meristem (SAM), which generates all the aerial parts of the plant. It has been known for many years that auxin plays a central role in the functioning of this meristem. Auxin is not homogeneously distributed at the SAM and it is thought that this distribution is interpreted in terms of differential gene expression and patterned growth. In this context, auxin transporters of the PIN and AUX families, creating auxin maxima and minima, are crucial regulators. However, auxin transport is not the only factor involved. Auxin biosynthesis genes also show specific, patterned activities, and local auxin synthesis appears to be essential for meristem function as well. In addition, auxin perception and signal transduction defining the competence of cells to react to auxin, add further complexity to the issue. To unravel this intricate signaling network at the SAM, systems biology approaches, involving not only molecular genetics but also live imaging and computational modeling, have become increasingly important.
Auxin dynamically regulates patterning at the shoot apical meristem. Transporters and local biosynthesis are involved in the control of its distribution at the shoot apex, where it is required for formation of new buds.
PMCID: PMC2845202  PMID: 20452945
9.  Localized auxin biosynthesis and postembryonic root development in Arabidopsis 
Plant Signaling & Behavior  2009;4(8):752-754.
Auxin is a phytohormone essential for plant development. Due to the high redundancy in auxin biosynthesis, the role of auxin biosynthesis in embryogenesis and seedling development, vascular and flower development, shade avoidance and ethylene response were revealed only recently. We previously reported that a vitamin B6 biosynthesis mutant pdx1 exhibits a short-root phenotype with reduced meristematic zone and short mature cells. By reciprocal grafting, we now have found that the pdx1 short root is caused by a root locally generated signal. The mutant root tips are defective in callus induction and have reduced DR5::GUS activity, but maintain relatively normal auxin response. Genetic analysis indicates that pdx1 mutant could suppress the root hair and root growth phenotypes of the auxin overproduction mutant yucca on medium supplemented with tryptophan (Trp), suggesting that the conversion from Trp to auxin is impaired in pdx1 roots. Here we present data showing that pdx1 mutant is more tolerant to 5-methyl anthranilate, an analogue of the Trp biosynthetic intermediate anthranilate, demonstrating that pdx1 is also defective in the conversion from anthranilate to auxin precursor tryptophan. Our data suggest that locally synthesized auxin may play an important role in the postembryonic root growth.
PMCID: PMC2801390  PMID: 19820306
auxin synthesis; root; PLP; PDX1
10.  A Regulatory Network for Coordinated Flower Maturation 
PLoS Genetics  2012;8(2):e1002506.
For self-pollinating plants to reproduce, male and female organ development must be coordinated as flowers mature. The Arabidopsis transcription factors AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 regulate this complex process by promoting petal expansion, stamen filament elongation, anther dehiscence, and gynoecium maturation, thereby ensuring that pollen released from the anthers is deposited on the stigma of a receptive gynoecium. ARF6 and ARF8 induce jasmonate production, which in turn triggers expression of MYB21 and MYB24, encoding R2R3 MYB transcription factors that promote petal and stamen growth. To understand the dynamics of this flower maturation regulatory network, we have characterized morphological, chemical, and global gene expression phenotypes of arf, myb, and jasmonate pathway mutant flowers. We found that MYB21 and MYB24 promoted not only petal and stamen development but also gynoecium growth. As well as regulating reproductive competence, both the ARF and MYB factors promoted nectary development or function and volatile sesquiterpene production, which may attract insect pollinators and/or repel pathogens. Mutants lacking jasmonate synthesis or response had decreased MYB21 expression and stamen and petal growth at the stage when flowers normally open, but had increased MYB21 expression in petals of older flowers, resulting in renewed and persistent petal expansion at later stages. Both auxin response and jasmonate synthesis promoted positive feedbacks that may ensure rapid petal and stamen growth as flowers open. MYB21 also fed back negatively on expression of jasmonate biosynthesis pathway genes to decrease flower jasmonate level, which correlated with termination of growth after flowers have opened. These dynamic feedbacks may promote timely, coordinated, and transient growth of flower organs.
Author Summary
Perfect flowers have both male organs that produce and release pollen and female organs that make and harbor seeds. Flowers also often attract pollinators using visual or chemical signals. So that male, female, and pollinator attraction functions occur at the right time, flower organs must grow and mature in a coordinated fashion. In the model self-pollinating plant Arabidopsis, a transcriptional network regulates genes that ensure coordinated growth of different flower organs, as well as pollen release and gynoecium (female) competence to support pollination. This network also regulates nectary development and production of volatile chemicals that may attract or repel insects. We have studied growth, chemical signal levels, and gene expression in mutants affected in components of this network, in order to determine how flower growth is controlled. Several plant hormones act in a cascade that promotes flower maturation. Moreover, regulatory feedback loops affect the timing and extent of developmental steps. Positive feedbacks may ensure that the development of different flower organs is coordinated and rapid, whereas negative feedbacks may allow growth to cease once flowers have opened. Our results provide a framework to understand how flower opening and reproduction are coordinated in Arabidopsis and other flowering plants.
PMCID: PMC3276552  PMID: 22346763
11.  Tissue-specific auxin signaling in response to temperature fluctuation 
Plant Signaling & Behavior  2010;5(11):1510-1512.
Auxin levels are well regulated in cells and tissues by both transport and local biosynthesis, and its distribution is important for the modulation of cell proliferation, differentiation, development, tropisms and high-temperature response. Activation of auxin biosynthesis with increased temperatures reported in certain plant tissues. In contrast, our studies indicated that male tissue-specific auxin reduction via transcriptional repression of the YUCCA auxin biosynthesis genes is the primary cause of high temperature injury, which leads the abortion of pollen development in Arabidopsis and barley Hordeum vulgare L. Furthermore, the abortion can be reversed by the application of exogenous auxin, suggesting that the application may maintain crop yields during the current global warming crisis.
PMCID: PMC3115269  PMID: 21051957
anther development; DR5-GUS; high temperature injury; male sterility; phytohormone
12.  Auxin biosynthesis and its role in plant development 
Indole-3-acetic acid (IAA), the main auxin in higher plants, has profound effects on plant growth and development. Both plants and some plant pathogens can produce IAA to modulate plant growth. While the genes and biochemical reactions for auxin biosynthesis in some plant pathogens are well understood, elucidation of the mechanisms by which plants produce auxin has proven to be difficult. So far, no complete pathway of de novo auxin biosynthesis in plants has been firmly established. However, recent studies have led to the discoveries of several genes in tryptophan dependent auxin biosynthesis pathways. Recent findings have also revealed that local auxin biosynthesis plays essential roles in many developmental processes including gametogenesis, embryogenesis, seedling growth, vascular patterning, and flower development. In this review, I summarize the recent advances in dissecting auxin biosynthetic pathways and how the understanding of auxin biosynthesis provides a different angle for analyzing the mechanisms of plant development.
PMCID: PMC3070418  PMID: 20192736
Arabidopsis; tryptophan; YUCCA; TAA1; flavin monooxygenase
13.  Over-expression of the IGI1 leading to altered shoot-branching development related to MAX pathway in Arabidopsis 
Plant Molecular Biology  2010;73(6):629-641.
Shoot branching and growth are controlled by phytohormones such as auxin and other components in Arabidopsis. We identified a mutant (igi1) showing decreased height and bunchy branching patterns. The phenotypes reverted to the wild type in response to RNA interference with the IGI1 gene. Histochemical analysis by GUS assay revealed tissue-specific gene expression in the anther and showed that the expression levels of the IGI1 gene in apical parts, including flowers, were higher than in other parts of the plants. The auxin biosynthesis component gene, CYP79B2, was up-regulated in igi1 mutants and the IGI1 gene was down-regulated by IAA treatment. These results indicated that there is an interplay regulation between IGI1 and phytohormone auxin. Moreover, the expression of the auxin-related shoot branching regulation genes, MAX3 and MAX4, was down-regulated in igi1 mutants. Taken together, these results indicate that the overexpression of the IGI1 influenced MAX pathway in the shoot branching regulation.
Electronic supplementary material
The online version of this article (doi:10.1007/s11103-010-9645-0) contains supplementary material, which is available to authorized users.
PMCID: PMC2898107  PMID: 20473553
Shoot branching; IGI1; MAX pathway
14.  High temperature injury and auxin biosynthesis in microsporogenesis 
Plant reproductive development is more sensitive than vegetative growth to many environmental stresses. High temperature (HT) injury is becoming an increasingly serious problem due to recent global warming. In wheat, barley, and other crops, the early phase of anther development is most susceptible to HT. I and my colleagues recently demonstrated that HT causes cell proliferation arrest and represses auxin signaling in a tissue-specific manner in the anther cells of barley and Arabidopsis. HT also caused comprehensive alterations in transcription. The application of auxin at the same time blocked the transcriptional alterations, led to the production of normal pollen grains, and restored the normal seed setting rate under increasing temperatures. Although synthetic auxins have been used widely as potent and selective herbicides, these recent results indicate that auxin is useful for the promotion of fertility and maintenance of crop yields under the threat of global warming.
PMCID: PMC3593198  PMID: 23483842
anther development; Arabidopsis; auxin; barley; high temperature injury; male sterility; tapetal degeneration; YUCCA
15.  Simulation of Organ Patterning on the Floral Meristem Using a Polar Auxin Transport Model 
PLoS ONE  2012;7(1):e28762.
An intriguing phenomenon in plant development is the timing and positioning of lateral organ initiation, which is a fundamental aspect of plant architecture. Although important progress has been made in elucidating the role of auxin transport in the vegetative shoot to explain the phyllotaxis of leaf formation in a spiral fashion, a model study of the role of auxin transport in whorled organ patterning in the expanding floral meristem is not available yet. We present an initial simulation approach to study the mechanisms that are expected to play an important role. Starting point is a confocal imaging study of Arabidopsis floral meristems at consecutive time points during flower development. These images reveal auxin accumulation patterns at the positions of the organs, which strongly suggests that the role of auxin in the floral meristem is similar to the role it plays in the shoot apical meristem. This is the basis for a simulation study of auxin transport through a growing floral meristem, which may answer the question whether auxin transport can in itself be responsible for the typical whorled floral pattern. We combined a cellular growth model for the meristem with a polar auxin transport model. The model predicts that sepals are initiated by auxin maxima arising early during meristem outgrowth. These form a pre-pattern relative to which a series of smaller auxin maxima are positioned, which partially overlap with the anlagen of petals, stamens, and carpels. We adjusted the model parameters corresponding to properties of floral mutants and found that the model predictions agree with the observed mutant patterns. The predicted timing of the primordia outgrowth and the timing and positioning of the sepal primordia show remarkable similarities with a developing flower in nature.
PMCID: PMC3264561  PMID: 22291882
16.  A role for the root cap in root branching revealed by the non-auxin probe naxillin 
Nature chemical biology  2012;8(9):798-805.
The acquisition of water and nutrients by plant roots is a fundamental aspect of agriculture and strongly depends on root architecture. Root branching and expansion of the root system is achieved through the development of lateral roots and is to a large extent controlled by the plant hormone auxin. However, the pleiotropic effects of auxin or auxin-like molecules on root systems complicate the study of lateral root development. Here we describe a small-molecule screen in Arabidopsis thaliana that identified naxillin as what is to our knowledge the first non-auxin-like molecule that promotes root branching. By using naxillin as a chemical tool, we identified a new function for root cap-specific conversion of the auxin precursor indole-3-butyric acid into the active auxin indole-3-acetic acid and uncovered the involvement of the root cap in root branching. Delivery of an auxin precursor in peripheral tissues such as the root cap might represent an important mechanism shaping root architecture.
PMCID: PMC3735367  PMID: 22885787
17.  Arabidopsis thaliana GH3.9 in Auxin and Jasmonate Cross Talk 
Plant Signaling & Behavior  2007;2(6):483-485.
Plant growth and development are governed by an intricate web of signaling networks controlled by phytohormones, such as auxin and jasmonic acid. Auxin influences all aspects of plant growth and development, ranging from embryogenesis to root and shoot morphogenesis and organ patterning. Three major groups of auxin-responsive genes have been classified as IAA/AUX, GH3 and SAUR families. Some Group I and II GH3 proteins biochemically function in conjugating amino acids to methyl jasmonate and auxin, respectively. We recently demonstrated that GH3.9, a previously uncharacterized Group II GH3 gene family member, influences primary root growth. Whereas several GH3 family members are transcriptionally induced by auxin, GH3.9 was repressed by exogenous indole-3-acetic acid (IAA) in whole seedlings. GH3.9 promoter::GUS reporter transgenic seedlings showed expression in several tissues, and application of exogenous IAA led to a shift in promoter activity from primary roots to lateral root tips, supporting the hypothesis that GH3.9 maintains auxin homeostasis by redistribution of active auxin pools in roots. GH3.9 mutations influenced both IAA- and methyl jasmonate (MeJA)-mediated root growth inhibition. In this addendum, we expand on a possible role for GH3.9 in crosstalk between auxin and jasmonate signal transduction pathways controlling plant development.
PMCID: PMC2634342  PMID: 19704592
amino acid conjugation; Arabidopsis thaliana; auxin; methyl jasmonate; trichomes; roots
18.  Expression of gibberellin 20-oxidase1 (AtGA20ox1) in Arabidopsis seedlings with altered auxin status is regulated at multiple levels 
Journal of Experimental Botany  2008;59(8):2057-2070.
Bioactive gibberellins (GAs) affect many biological processes including germination, stem growth, transition to flowering, and fruit development. The location, timing, and level of bioactive GA are finely tuned to ensure that optimal growth and development occur. The balance between GA biosynthesis and deactivation is controlled by external factors such as light and by internal factors that include auxin. The role of auxin transport inhibitors (ATIs) and auxins on GA homeostasis in intact light-grown Arabidopsis thaliana (L.) Heynh. seedlings was investigated. Two ATIs, 1-N-naphthylthalamic acid (NPA) and 1-naphthoxyacetic acid (NOA) caused elevated expression of the GA biosynthetic enzyme AtGA20-oxidase1 (AtGA20ox1) in shoot but not in root tissues, and only at certain developmental stages. It was investigated whether enhanced AtGA20ox1 gene expression was a consequence of altered flow through the GA biosynthetic pathway, or was due to impaired GA signalling that can lead to enhanced AtGA20ox1 expression and accumulation of a DELLA protein, Repressor of ga1-3 (RGA). Both ATIs promoted accumulation of GFP-fused RGA in shoots and roots, and this increase was counteracted by the application of GA4. These results suggest that in ATI-treated seedlings the impediment to DELLA protein degradation may be a deficiency of bioactive GA at sites of GA response. It is proposed that the four different levels of AtGA20ox1 regulation observed here are imposed in a strict hierarchy: spatial (organ-, tissue-, cell-specific) > developmental > metabolic > auxin regulation. Thus results show that, in intact auxin- and auxin transport inhibitor-treated light-grown Arabidopsis seedlings, three other levels of regulation supersede the effects of auxin on AtGA20ox1.
PMCID: PMC2413289  PMID: 18440929
Auxin; auxin transport inhibitors; DELLA proteins; gibberellin 20-oxidase; gibberellin biosynthesis; RGA
19.  The role of auxin in style development and apical-basal patterning of the Arabidopsis thaliana gynoecium 
Plant Signaling & Behavior  2009;4(2):83-85.
In angiosperms, the gynoecium constitutes the female reproductive organ that after fertilization develops into a fruit and in Arabidopsis thaliana the gynoecium is formed by the congenital fusion of two carpels. In the last few years many genes involved in female organ development have been identified and there have been several reports on the involvement of the plant hormone auxin in gynoecium patterning. An auxin gradient has been suggested to establish the apical-basal patterning of the gynoecium and recently it has been shown that elevated apical auxin levels can compensate for the loss of several style-promoting factors but that auxin is dependent on their action in apical-basal patterning. Here we discuss the role of auxin and different upstream, downstream or parallel factors in the apical-basal patterning of the gynoecium. We focus specifically on the development of style and stigma and discuss the most recent findings.
PMCID: PMC2637486  PMID: 19649177
auxin; fruit; gynoecium; style; STYLISH1; PAT; NPA
20.  Evolution and Structural Diversification of PILS Putative Auxin Carriers in Plants 
The phytohormone auxin contributes to virtually every aspect of the plant development. The spatiotemporal distribution of auxin depends on a complex interplay between auxin metabolism and intercellular auxin transport. Intracellular auxin compartmentalization provides another link between auxin transport processes and auxin metabolism. The PIN-LIKES (PILS) putative auxin carriers localize to the endoplasmic reticulum (ER) and contribute to cellular auxin homeostasis. PILS proteins regulate intracellular auxin accumulation, the rate of auxin conjugation and, subsequently, affect nuclear auxin signaling. Here, we investigate sequence diversification of the PILS family in Arabidopsis thaliana and provide insights into the evolution of these novel putative auxin carriers in plants. Our data suggest that PILS proteins are conserved throughout the plant lineage and expanded during higher plant evolution. PILS proteins diversified early during plant evolution into three clades. Besides the ancient Clade I encompassing non-land plant species, PILS proteins evolved into two clades. The diversification of Clade II and Clade III occurred already at the level of non-vascular plant evolution and, hence, both clades contain vascular and non-vascular plant species. Nevertheless, Clade III contains fewer non- and increased numbers of vascular plants, indicating higher importance of Clade III for vascular plant evolution. Notably, PILS proteins are distinct and appear evolutionarily older than the prominent PIN-FORMED auxin carriers. Moreover, we revealed particular PILS sequence divergence in Arabidopsis and assume that these alterations could contribute to distinct gene regulations and protein functions.
PMCID: PMC3470039  PMID: 23091477
PILS proteins; auxin; evolution; phylogeny; auxin metabolism; auxin homeostasis
21.  Down-regulation of a single auxin efflux transport protein in tomato induces precocious fruit development 
Journal of Experimental Botany  2012;63(13):4901-4917.
The PIN-FORMED (PIN) auxin efflux transport protein family has been well characterized in the model plant Arabidopsis thaliana, where these proteins are crucial for auxin regulation of various aspects of plant development. Recent evidence indicates that PIN proteins may play a role in fruit set and early fruit development in tomato (Solanum lycopersicum), but functional analyses of PIN-silenced plants failed to corroborate this hypothesis. Here it is demonstrated that silencing specifically the tomato SlPIN4 gene, which is predominantly expressed in tomato flower bud and young developing fruit, leads to parthenocarpic fruits due to precocious fruit development before fertilization. This phenotype was associated with only slight modifications of auxin homeostasis at early stages of flower bud development and with minor alterations of ARF and Aux/IAA gene expression. However, microarray transcriptome analysis and large-scale quantitative RT-PCR profiling of transcription factors in developing flower bud and fruit highlighted differentially expressed regulatory genes, which are potential targets for auxin control of fruit set and development in tomato. In conclusion, this work provides clear evidence that the tomato PIN protein SlPIN4 plays a major role in auxin regulation of tomato fruit set, possibly by preventing precocious fruit development in the absence of pollination, and further gives new insights into the target genes involved in fruit set.
PMCID: PMC3427993  PMID: 22844095
Auxin efflux transport protein (PIN);  CRABS-CLAW;  fruit set;  MADS-BOX;  parthenocarpy;  tomato (Solanum lycopersicum);  transcription factor
22.  The Circadian Clock Regulates Auxin Signaling and Responses in Arabidopsis 
PLoS Biology  2007;5(8):e222.
The circadian clock plays a pervasive role in the temporal regulation of plant physiology, environmental responsiveness, and development. In contrast, the phytohormone auxin plays a similarly far-reaching role in the spatial regulation of plant growth and development. Went and Thimann noted 70 years ago that plant sensitivity to auxin varied according to the time of day, an observation that they could not explain. Here we present work that explains this puzzle, demonstrating that the circadian clock regulates auxin signal transduction. Using genome-wide transcriptional profiling, we found many auxin-induced genes are under clock regulation. We verified that endogenous auxin signaling is clock regulated with a luciferase-based assay. Exogenous auxin has only modest effects on the plant clock, but the clock controls plant sensitivity to applied auxin. Notably, we found both transcriptional and growth responses to exogenous auxin are gated by the clock. Thus the circadian clock regulates some, and perhaps all, auxin responses. Consequently, many aspects of plant physiology not previously thought to be under circadian control may show time-of-day–specific sensitivity, with likely important consequences for plant growth and environmental responses.
Author Summary
Most higher organisms, including plants and animals, have developed a time-keeping mechanism that allows them to anticipate daily fluctuations of environmental parameters such as light and temperature. This circadian clock efficiently coordinates plant growth and metabolism with respect to time of day by producing self-sustained rhythms of gene expression with an approximately 24-h period. One of the major contributors in specifying spatial patterns of plant growth and development is auxin, a hormone essential for nearly all stages of plant development. Auxin also helps the plant orient itself properly in response to environmental cues such as light, gravity, and water. We have now found circadian-regulated expression of components from nearly every step in the auxin-signaling pathway, from synthesis to response. We demonstrate the relevance of this observation by showing that plants have differential sensitivity to auxin at different times of day: the clock controls plant sensitivity to auxin at both the level of transcription and stem growth. Our work demonstrates an intimate connection between the clock- and auxin-signaling pathways, and suggests that other auxin-regulated processes may also be under circadian control.
The circadian regulation of auxin responses suggests that many aspects of plant physiology not previously thought to be under circadian control may show time-of-day-specific sensitivity.
PMCID: PMC1939880  PMID: 17683202
23.  Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance 
Annals of Botany  2012;110(2):349-360.
Background and Aims
The root apical meristem (RAM) is the plant stem cell niche which provides for the formation and continuous development of the root. Auxin is the main regulator of RAM functioning, and auxin maxima coincide with the sites of RAM initiation and maintenance. Auxin gradients are formed due to local auxin biosynthesis and polar auxin transport. The PIN family of auxin transporters plays a critical role in polar auxin transport, and two mechanisms of auxin maximum formation in the RAM based on PIN-mediated auxin transport have been proposed to date: the reverse fountain and the reflected flow mechanisms.
The two mechanisms are combined here in in silico studies of auxin distribution in intact roots and roots cut into two pieces in the proximal meristem region. In parallel, corresponding experiments were performed in vivo using DR5::GFP Arabidopsis plants.
Key Results
The reverse fountain and the reflected flow mechanism naturally cooperate for RAM patterning and maintenance in intact root. Regeneration of the RAM in decapitated roots is provided by the reflected flow mechanism. In the excised root tips local auxin biosynthesis either alone or in cooperation with the reverse fountain enables RAM maintenance.
The efficiency of a dual-mechanism model in guiding biological experiments on RAM regeneration and maintenance is demonstrated. The model also allows estimation of the concentrations of auxin and PINs in root cells during development and under various treatments. The dual-mechanism model proposed here can be a powerful tool for the study of several different aspects of auxin function in root.
PMCID: PMC3394645  PMID: 22510326
Auxin response; root apical meristem; patterning; reverse fountain; reflected flow; mathematical model; Arabidopsis thaliana
24.  The evolution of nuclear auxin signalling 
The plant hormone auxin directs many aspects of plant growth and development. To understand the evolution of auxin signalling, we compared the genes encoding two families of crucial transcriptional regulators, AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA), among flowering plants and two non-seed plants, Physcomitrella patens and Selaginella moellendorffii.
Comparative analysis of the P. patens, S. moellendorffii and Arabidopsis thaliana genomes suggests that the well-established rapid transcriptional response to auxin of flowering plants, evolved in vascular plants after their divergence from the last common ancestor shared with mosses. An N-terminally truncated ARF transcriptional activator is encoded by the genomes of P. patens and S. moellendorffii, and suggests a supplementary mechanism of nuclear auxin signalling, absent in flowering plants. Site-specific analyses of positive Darwinian selection revealed relatively high rates of synonymous substitution in the A. thaliana ARFs of classes IIa (and their closest orthologous genes in poplar) and Ib, suggesting that neofunctionalization in important functional regions has driven the evolution of auxin signalling in flowering plants. Primary auxin responsive gene families (GH3, SAUR, LBD) show different phylogenetic profiles in P. patens, S. moellendorffii and flowering plants, highlighting genes for further study.
The genome of P. patens encodes all of the basic components necessary for a rapid auxin response. The spatial separation of the Q-rich activator domain and DNA-binding domain suggests an alternative mechanism of transcriptional control in P. patens distinct from the mechanism seen in flowering plants. Significantly, the genome of S. moellendorffii is predicted to encode proteins suitable for both methods of regulation.
PMCID: PMC2708152  PMID: 19493348
25.  Defining Binding Efficiency and Specificity of Auxins for SCFTIR1/AFB-Aux/IAA Co-receptor Complex Formation 
ACS Chemical Biology  2013;9(3):673-682.
Structure–activity profiles for the phytohormone auxin have been collected for over 70 years, and a number of synthetic auxins are used in agriculture. Auxin classification schemes and binding models followed from understanding auxin structures. However, all of the data came from whole plant bioassays, meaning the output was the integral of many different processes. The discovery of Transport Inhibitor-Response 1 (TIR1) and the Auxin F-Box (AFB) proteins as sites of auxin perception and the role of auxin as molecular glue in the assembly of co-receptor complexes has allowed the development of a definitive quantitative structure–activity relationship for TIR1 and AFB5. Factorial analysis of binding activities offered two uncorrelated factors associated with binding efficiency and binding selectivity. The six maximum-likelihood estimators of Efficiency are changes in the overlap matrixes, inferring that Efficiency is related to the volume of the electronic system. Using the subset of compounds that bound strongly, chemometric analyses based on quantum chemical calculations and similarity and self-similarity indices yielded three classes of Specificity that relate to differential binding. Specificity may not be defined by any one specific atom or position and is influenced by coulomb matrixes, suggesting that it is driven by electrostatic forces. These analyses give the first receptor-specific classification of auxins and indicate that AFB5 is the preferred site for a number of auxinic herbicides by allowing interactions with analogues having van der Waals surfaces larger than that of indole-3-acetic acid. The quality factors are also examined in terms of long-standing models for the mechanism of auxin binding.
PMCID: PMC3964829  PMID: 24313839

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