An Auxin-Mediated Shift toward Growth Isotropy Promotes Organ Formation at the Shoot Meristem in Arabidopsis

Sassi, Massimiliano; Ali, Olivier; Boudon, Frédéric; Cloarec, Gladys; Abad, Ursula; Cellier, Coralie; Chen, Xu; Gilles, Benjamin; Milani, Pascale; Friml, Jiřı́; Vernoux, Teva; Godin, Christophe; Hamant, Olivier; Traas, Jan

doi:10.1016/j.cub.2014.08.036

Cited by 135 publications

(149 citation statements)

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“…Sassi et al (30) showed that chemical or genetic perturbation of cortical microtubules restores some primordia initiation in pin1 mutants as well as in naphtylphtalamic acid (NPA)-treated Arabidopsis apices, suggesting that auxin is not the only factor directing organ formation and that, although it is sufficient for initiation, it might not be necessary. Indeed, in Arabidopsis pin1 and pid mutants, abolishment of lateral organ initiation is restricted to the bolting stem, whereas rosette leaves develop quite normally (4,7,31), questioning the unique contribution of auxin regulatory mechanisms to primordia initiation.…”

Section: Discussionmentioning

confidence: 99%

Coordination of auxin-triggered leaf initiation by tomato LEAFLESS

Capua

Eshed

2017

Proc. Natl. Acad. Sci. U.S.A.

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Lateral plant organs, particularly leaves, initiate at the flanks of the shoot apical meristem (SAM) following auxin maxima signals; however, little is known about the underlying mechanisms. Here, we show that tomato leafless (lfs) mutants fail to produce cotyledons and leaves and grow a naked pin while maintaining an active SAM. A similar phenotype was observed among pin-like shoots induced by polar auxin transport inhibitors such as 2,3,5-triiodobenzoic acid (TIBA). Both types of pin-like shoots showed reduced expression of primordia markers as well as abnormal auxin distribution, as evidenced by expression of the auxin reporters pPIN1: PIN1:GFP and DR5:YFP. Upon auxin microapplication, both lfs meristems and TIBA-pin apices activated DR5:YFP expression with similar kinetics; however, only lfs plants failed to concurrently initiate leaf primordia. We found that LFS encodes the single tomato ortholog of Arabidopsis DORNRONSCHEN (DRN) and DRN-like (DRNL) genes and is transiently expressed at incipient and young primordia, overlapping with auxin response maxima. LFS is rapidly induced by auxin application, implying feed-forward activity between LFS and auxin signals. However, driving LFS at auxin response maxima sites using the DR5 promoter fails to fully rescue lfs plants, suggesting that additional, auxin-independent regulation is needed. Indeed, extended GCC-box elements upstream of LFS drove primordia-specific expression in a LFS-dependent but auxin-independent manner. We thus suggest that LFS transiently acts at the site of primordia initiation, where it provides a specific context to auxin response maxima culminating in leaf primordia initiation.L ateral aerial plant organs form at the flanks of the shoot apical meristem (SAM) in a species-specific order termed phyllotaxis. Phyllotactic patterns tightly correlate with local maxima of the phytohormone auxin at the SAM periphery (1-3). These maxima are achieved by active transport (4). At these sites, auxin is required for leaf initiation, and when polar auxin transport is chemically impaired by polar auxin transport inhibitors (PATI), leaves fail to form (5-7), resulting in a pin-like shoot. When auxin is externally applied onto the meristem of these pins or to the meristem in a wild-type (WT) background, leaf primordia are initiated (5). Genetic analyses have also demonstrated that auxin response maxima, dictated by the activity of the auxin efflux carrier PINFORMED1 (PIN1), can be detected before, and are required for, leaflet initiation in compound leaves (6). However, similar evidence for leaf initiation is lacking (7).Like other classical hormones, such as cytokinin (CK), florigen, and gibberellin, auxin has many functions, which are largely dictated by its levels and which vary within and among plants. In young leaf primordia, auxin triggers primordia bulging at P 0 by stimulating local cell divisions. At P 1 and P 2 , auxin elicits provasculature development (8). Thus, in the same group of cells, auxin cues are differentially translated to cell divisi...

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Section: Discussionmentioning

confidence: 99%

Coordination of auxin-triggered leaf initiation by tomato LEAFLESS

Capua

Eshed

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…When cortical MT arrays in longitudinally expanding cells are formed in an oblique orientation, due to MT-related mutations or treatment with MT-targeted drugs, the growth direction is tilted perpendicular to the MT alignment (Hashimoto, 2011). On the other hand, well-aligned transverse MT arrays appear to restrain auxin-mediated organ initiation at the shoot meristem in Arabidopsis (Sassi et al, 2014). In the trichoblast cells of Lactuca sativa (lettuce) roots, root hair initiation is suppressed by ordered arrays of cortical MTs (Takahashi et al, 2003).…”

Section: Plant Mt Arrays Interphase Arraysmentioning

confidence: 99%

Microtubules in Plants

Hashimoto

2015

The Arabidopsis Book

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Microtubules (MTs) are highly conserved polar polymers that are key elements of the eukaryotic cytoskeleton and are essential for various cell functions. αβ-tubulin, a heterodimer containing one structural GTP and one hydrolysable and exchangeable GTP, is the building block of MTs and is formed by the sequential action of several molecular chaperones. GTP hydrolysis in the MT lattice is mechanistically coupled with MT growth, thus giving MTs a metastable and dynamic nature. MTs adopt several distinct higher-order organizations that function in cell division and cell morphogenesis. Small molecular weight compounds that bind tubulin are used as herbicides and as research tools to investigate MT functions in plant cells. The de novo formation of MTs in cells requires conserved γ-tubulin-containing complexes and targeting/activating regulatory proteins that contribute to the geometry of MT arrays. Various MT regulators and tubulin modifications control the dynamics and organization of MTs throughout the cell cycle and in response to developmental and environmental cues. Signaling pathways that converge on the regulation of versatile MT functions are being characterized.

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“…Experiments demonstrating auxin binding activity for ABP1 were published as early as the 1980s (reviewed in Jones, 1994). Reverse genetics proved to be a complicated approach to study ABP1 function in Arabidopsis thaliana, as two independently generated abp1 mutants, presumed to be null alleles, appeared to be embryo lethal (Chen et al, 2001;Tzafrir et al, 2004;Meinke et al, 2008;Sassi et al, 2014). Knockdown lines of ABP1 provided some ability to study ABP1 function by reverse genetics.…”

Section: Introductionmentioning

confidence: 99%

Genome Sequencing of Arabidopsis abp1-5 Reveals Second-Site Mutations That May Affect Phenotypes

Enders

Yang

et al. 2015

The Plant Cell

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Auxin regulates numerous aspects of plant growth and development. For many years, investigating roles for AUXIN BINDING PROTEIN1 (ABP1) in auxin response was impeded by the reported embryo lethality of mutants defective in ABP1. However, identification of a viable Arabidopsis thaliana TILLING mutant defective in the ABP1 auxin binding pocket (abp1-5) allowed inroads into understanding ABP1 function. During our own studies with abp1-5, we observed growth phenotypes segregating independently of the ABP1 lesion, leading us to sequence the genome of the abp1-5 line described previously. We found that the abp1-5 line we sequenced contains over 8000 single nucleotide polymorphisms in addition to the ABP1 mutation and that at least some of these mutations may originate from the Arabidopsis Wassilewskija accession. Furthermore, a phyB null allele in the abp1-5 background is likely causative for the long hypocotyl phenotype previously attributed to disrupted ABP1 function. Our findings complicate the interpretation of abp1-5 phenotypes for which no complementation test was conducted. Our findings on abp1-5 also provide a cautionary tale illustrating the need to use multiple alleles or complementation lines when attributing roles to a gene product. INTRODUCTIONThe plant hormone auxin regulates cell division and cell expansion to affect all aspects of plant growth (reviewed in PerrotRechenmann, 2010). Auxin regulates a wide range of developmental processes, and tight control of auxin response is maintained by multiple modes of regulation. These include regulating auxin biosynthesis and metabolism, transport, and signaling (reviewed in Enders and Strader, 2015). To date, nuclear auxin signaling components have been well characterized (reviewed in Chapman and Estelle, 2009;Salehin et al., 2015). In addition, a nontranscriptional auxin response pathway has been proposed, with AUXIN BINDING PROTEIN1 (ABP1) acting in the apoplast as an auxin receptor and transmitting a cytoplasmic signal to regulate auxin responses such as auxin transport and cytoskeletal rearrangements (reviewed in Shi and Yang, 2011;Sauer et al., 2013).Study of ABP1 has a long, complicated history. Experiments demonstrating auxin binding activity for ABP1 were published as early as the 1980s (reviewed in Jones, 1994). Reverse genetics proved to be a complicated approach to study ABP1 function in Arabidopsis thaliana, as two independently generated abp1 mutants, presumed to be null alleles, appeared to be embryo lethal (Chen et al., 2001;Tzafrir et al., 2004;Meinke et al., 2008;Sassi et al., 2014). Knockdown lines of ABP1 provided some ability to study ABP1 function by reverse genetics. Arabidopsis lines expressing an inducible ABP1 antisense transcript or an inducible single-chain fragment variable scFv12 (David et al., 2007) from a monoclonal antibody raised to ABP1 (Leblanc et al., 1999), targeted to either the apoplast (SS12S) or the endoplasmic reticulum (SS12K), led to phenotypes consistent with decreased auxin activity (Braun et al., 2008;Tromas et al.,...

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An Auxin-Mediated Shift toward Growth Isotropy Promotes Organ Formation at the Shoot Meristem in Arabidopsis

Cited by 135 publications

References 35 publications

Coordination of auxin-triggered leaf initiation by tomato LEAFLESS

Coordination of auxin-triggered leaf initiation by tomato LEAFLESS

Microtubules in Plants

Genome Sequencing of Arabidopsis abp1-5 Reveals Second-Site Mutations That May Affect Phenotypes

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