<i>AUX/LAX</i> Genes Encode a Family of Auxin Influx Transporters That Perform Distinct Functions during <i>Arabidopsis</i> Development

Péret, Benjamin; Swarup, Kamal; Ferguson, Alison; Seth, Malvika; Yang, Yaodong; Dhondt, Stijn; James, Nicholas D.; Casimiro, Ilda; Perry, Paula; Syed, Adnan K.; Yang, Haibing; Reemmer, Jesica; Venison, Edward; Howells, Caroline; Pérez‐Amador, Miguel A.; Yun, Jeonga; Alonso, José M.; Beemster, Gerrit T.S.; Laplaze, Laurent; Murphy, Angus S.; Bennett, Malcolm J.; Nielsen, Erik; Swarup, Ranjan

doi:10.1105/tpc.112.097766

Cited by 382 publications

(399 citation statements)

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“…We showed that genetic and localized chemical inhibition of auxin transport significantly affected regeneration. Despite known redundancy among auxin transporters (Blilou et al, 2005;Péret et al, 2012), we detected phenotypes in single mutants, suggesting spatial compartmentalization. Supporting this idea, PIN-FORMED3 (PIN3) was expressed in the petiole vasculature whereas PIN4 was later restricted to the proliferating vascular region.…”

Section: Vasculature Proliferation and Endogenous Callus Formationmentioning

confidence: 90%

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

et al. 2017

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Body regeneration through formation of new organs is a major question in developmental biology. We investigated de novo root formation using whole leaves of Arabidopsis (Arabidopsis thaliana). Our results show that local cytokinin biosynthesis and auxin biosynthesis in the leaf blade followed by auxin long-distance transport to the petiole leads to proliferation of J0121-marked xylem-associated tissues and others through signaling of INDOLE-3-ACETIC ACID INDUCIBLE28 (IAA28), CRANE (IAA18), WOODEN LEG, and ARABIDOPSIS RESPONSE REGULATORS1 (ARR1), ARR10, and ARR12. Vasculature proliferation also involves the cell cycle regulator KIP-RELATED PROTEIN2 and ABERRANT LATERAL ROOT FORMATION4, resulting in a mass of cells with rooting competence that resembles callus formation. Endogenous callus formation precedes specification of postembryonic root founder cells, from which roots are initiated through the activity of SHORT-ROOT, PLETHORA1 (PLT1), and PLT2. Primordia initiation is blocked in shr plt1 plt2 mutant. Stem cell regulators SCHIZORIZA, JACKDAW, BLUEJAY, and SCARECROW also participate in root initiation and are required to pattern the new organ, as mutants show disorganized and reduced number of layers and tissue initials resulting in reduced rooting. Our work provides an organ regeneration model through de novo root formation, stating key stages and the primary pathways involved.Plants have striking regeneration capacities, and can produce new organs from postembryonic tissues (Hartmann et al., 2010;Chen et al., 2014;Liu et al., 2014) as well as reconstitute damaged organs upon wounding (Xu et al., 2006;Heyman et al., 2013; PerianezRodriguez et al., 2014;Melnyk et al., 2015;Efroni et al., 2016). Intriguingly, root regeneration upon stem cell damage recruits embryonic pathways (Hayashi et al., 2006;Efroni et al., 2016), whereas in contrast, postembryonic formation of whole new organs, such as lateral roots, appears to use specific postembryonic pathways (Lavenus et al., 2013).Cross talk between auxin and cytokinin signaling is required for many aspects of plant development and regeneration (El-Showk et al., 2013), although how their synergistic interaction is implemented at the molecular level has not been clarified (Skoog and Miller, 1957;Chandler and Werr, 2015). Exogenous in vitro supplementation of these two hormones results in continuous cell proliferation, to form a characteristic structure termed "callus". Callus emerges as a common regenerative mechanism for almost all plant organs through in vitro culture (Atta et al., 2009;Sugimoto et al., 2010). There is increasing evidence that callus formation requires hormone-mediated activation of a lateral and meristematic root development program in pericycle-like cells defined by expression of the J0121 marker 1 This work was supported by grants from Ministerio de Economía y Competitividad (MINECO) of Spain, the European Regional Development Fund (ERDF) and FP7 Funds of the European Commission, BFU2013-41160-P, BFU2016-80315-P, and PCIG11-GA-2012-322082 to M.A....

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Section: Vasculature Proliferation and Endogenous Callus Formationmentioning

confidence: 90%

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

et al. 2017

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“…IAA is protonated in the acidic apoplast and deprotonated in the weakly basic cytosol. Uptake of the uncharged molecule occurs by AUX1/LAX (auxin1/like AUX1) uptake carriers (Péret et al, 2012) in an undirected way. Extrusion of negatively charged IAA occurs via undirected ABCB transporter-mediated efflux (Noh et al, 2001;Geisler et al, 2005) and by PIN (pin-formed) proteins that are responsible for directed auxin movement (Friml et al, 2003;Blilou et al, 2005).…”

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confidence: 99%

Root Bending Is Antagonistically Affected by Hypoxia and ERF-Mediated Transcription via Auxin Signaling

Eysholdt-Derzsó

Sauter

2017

Plant Physiol.

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ORCID ID: 0000-0002-7370-643X (M.S.).When plants encounter soil water logging or flooding, roots are the first organs to be confronted with reduced gas diffusion resulting in limited oxygen supply. Since roots do not generate photosynthetic oxygen, they are rapidly faced with oxygen shortage rendering roots particularly prone to damage. While metabolic adaptations to low oxygen conditions, which ensure basic energy supply, have been well characterized, adaptation of root growth and development have received less attention. In this study, we show that hypoxic conditions cause the primary root to grow sidewise in a low oxygen environment, possibly to escape soil patches with reduced oxygen availability. This growth behavior is reversible in that gravitropic growth resumes when seedlings are returned to normoxic conditions. Hypoxic root bending is inhibited by the group VII ethylene response factor (ERFVII) RAP2.12, as rap2.12-1 seedlings show exaggerated primary root bending. Furthermore, overexpression of the ERFVII member HRE2 inhibits root bending, suggesting that primary root growth direction at hypoxic conditions is antagonistically regulated by hypoxia and hypoxia-activated ERFVIIs. Root bending is preceded by the establishment of an auxin gradient across the root tip as quantified with DII-VENUS and is synergistically enhanced by hypoxia and the auxin transport inhibitor naphthylphthalamic acid. The protein abundance of the auxin efflux carrier PIN2 is reduced at hypoxic conditions, a response that is suppressed by RAP2.12 overexpression, suggesting antagonistic control of auxin flux by hypoxia and ERFVII. Taken together, we show that hypoxia triggers an escape response of the primary root that is controlled by ERFVII activity and mediated by auxin signaling in the root tip.

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“…Proper plant development strictly requires the directed cell-to-cell transport of auxin, which is achieved by a system of auxin influx and efflux transporters (1). AUXIN RESISTANT1 (AUX1)/LIKE-AUX1 (LAX) proteins are auxin influx transporters and PIN-FORMED (PIN) proteins are auxin efflux transporters that may act together with ABC transporters (3)(4)(5)(6)(7)(8). Auxin transport gains its directionality through the often polar distribution of the plasma membrane-resident PIN auxin efflux carriers, PIN1-PIN4 and PIN7 in Arabidopsis thaliana (1,9).…”

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confidence: 99%

Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth

Weller

Zourelidou

Frank

et al. 2017

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

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The directional distribution of the phytohormone auxin is essential for plant development. Directional auxin transport is mediated by the polarly distributed PIN-FORMED (PIN) auxin efflux carriers. We have previously shown that efficient PIN1-mediated auxin efflux requires activation through phosphorylation at the four serines S1-S4 in Arabidopsis thaliana. The Brefeldin A (BFA)-sensitive D6 PROTEIN KINASE (D6PK) and the BFA-insensitive PINOID (PID) phosphorylate and activate PIN1 through phosphorylation at all four phosphosites. PID, but not D6PK, can also induce PIN1 polarity shifts, seemingly through phosphorylation at S1-S3. The differential effects of D6PK and PID on PIN1 polarity had so far been attributed to their differential phosphosite preference for the four PIN1 phosphosites. We have mapped PIN1 phosphorylation at S1-S4 in situ using phosphosite-specific antibodies. We detected phosphorylation at PIN1 phosphosites at the basal (rootward) as well as the apical (shootward) plasma membrane in different root cell types, in embryos, and shoot apical meristems. Thereby, PIN1 phosphorylation at all phosphosites generally followed the predominant PIN1 distribution but was not restricted to specific polar sides of the cells. PIN1 phosphorylation at the basal and apical plasma membrane was differentially sensitive to BFA treatments, suggesting the involvement of different protein kinases or trafficking mechanisms in PIN1 phosphorylation control. We conclude that phosphosite preferences are not sufficient to explain the differential effects of D6PK and PID on PIN1 polarity, and suggest that a more complex model is needed to explain the effects of PID.auxin transport | protein kinase | Arabidopsis | PIN1 | polarity T he phytohormone auxin is a central regulator of plant development and tropic growth (1, 2). Proper plant development strictly requires the directed cell-to-cell transport of auxin, which is achieved by a system of auxin influx and efflux transporters (1). AUXIN RESISTANT1 (AUX1)/LIKE-AUX1 (LAX) proteins are auxin influx transporters and PIN-FORMED (PIN) proteins are auxin efflux transporters that may act together with ABC transporters (3-8). Auxin transport gains its directionality through the often polar distribution of the plasma membrane-resident PIN auxin efflux carriers, PIN1-PIN4 and PIN7 in Arabidopsis thaliana (1, 9). Directional auxin transport results in the formation of cellular auxin maxima and minima that provide essential cues for plant growth and differentiation at the level of individual cells and tissues (1, 2). PIN1 localizes to the basal (rootward) plasma membrane in root stele cells and directs auxin transport toward the root tip (3). PIN2 localizes differentially to the basal (rootward) and apical (shootward) plasma membrane in cortex and epidermis cells, respectively, and the opposing auxin transport streams in cortex and epidermis are important for gravitropic root growth (10, 11).Efficient PIN1-mediated auxin efflux requires activation by phosphorylation (12, 13). In the case...

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AUX/LAX Genes Encode a Family of Auxin Influx Transporters That Perform Distinct Functions during Arabidopsis Development

Cited by 382 publications

References 32 publications

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

Regulation of Hormonal Control, Cell Reprogramming, and Patterning during De Novo Root Organogenesis

Root Bending Is Antagonistically Affected by Hypoxia and ERF-Mediated Transcription via Auxin Signaling

Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth

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