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Wenkun Zhou,
Lirong Wei, Jian Xu,
Qingzhe Zhai,
Hongling Jiang,
Rong Chen,
Qian Chen,
Jiaqiang Sun,
Jinfang Chu,
Lihuang Zhu,
Chun-Ming Liu,
Chuanyou Li
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ABSTRACT: Recent identification of the Arabidopsis thaliana tyrosylprotein sulfotransferase (TPST) and a group of Tyr-sulfated peptides known as root meristem growth factors (RGFs) highlights the importance of protein Tyr sulfation in plant growth and development. Here, we report the action mechanism of TPST in maintenance of the root stem cell niche, which in the Arabidopsis root meristem is an area of four mitotically inactive quiescent cells plus the surrounding mitotically active stem cells. Mutation of TPST leads to defective maintenance of the root stem cell niche, decreased meristematic activity, and stunted root growth. We show that TPST expression is positively regulated by auxin and that mutation of this gene affects auxin distribution by reducing local expression levels of several PIN genes and auxin biosynthetic genes in the stem cell niche region. We also show that mutation of TPST impairs basal- and auxin-induced expression of the PLETHORA (PLT) stem cell transcription factor genes and that overexpression of PLT2 rescues the root meristem defects of the loss-of-function mutant of TPST. Together, these results support that TPST acts to maintain root stem cell niche by regulating basal- and auxin-induced expression of PLT1 and PLT2. TPST-dependent sulfation of RGFs provides a link between auxin and PLTs in regulating root stem cell niche maintenance.
The Plant Cell 11/2010; 22(11):3692-709. · 8.99 Impact Factor
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Pankaj Dhonukshe,
Fang Huang,
Carlos S Galvan-Ampudia,
Ari Pekka Mähönen,
Jurgen Kleine-Vehn, Jian Xu,
Ab Quint,
Kalika Prasad,
Jirí Friml,
Ben Scheres,
Remko Offringa
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ABSTRACT: Polar membrane cargo delivery is crucial for establishing cell polarity and for directional transport processes. In plants, polar trafficking mediates the dynamic asymmetric distribution of PIN FORMED (PIN) carriers, which drive polar cell-to-cell transport of the hormone auxin, thereby generating auxin maxima and minima that control development. The Arabidopsis PINOID (PID) protein kinase instructs apical PIN localization by phosphorylating PINs. Here, we identified the PID homologs WAG1 and WAG2 as new PIN polarity regulators. We show that the AGC3 kinases PID, WAG1 and WAG2, and not other plant AGC kinases, instruct recruitment of PINs into the apical recycling pathway by phosphorylating the middle serine in three conserved TPRXS(N/S) motifs within the PIN central hydrophilic loop. Our results put forward a model by which apolarly localized PID, WAG1 and WAG2 phosphorylate PINs at the plasma membrane after default non-polar PIN secretion, and trigger endocytosis-dependent apical PIN recycling. This phosphorylation-triggered apical PIN recycling competes with ARF-GEF GNOM-dependent basal recycling to promote apical PIN localization. In planta, expression domains of PID, WAG1 and WAG2 correlate with apical localization of PINs in those cell types, indicating the importance of these kinases for apical PIN localization. Our data show that by directing polar PIN localization and PIN-mediated polar auxin transport, the three AGC3 kinases redundantly regulate cotyledon development, root meristem size and gravitropic response, indicating their involvement in both programmed and adaptive plant development.
Development 10/2010; 137(19):3245-55. · 6.60 Impact Factor
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ABSTRACT: Because plant cells do not migrate, cell division planes are crucial determinants of plant cellular architecture. In Arabidopsis roots, stringent control of cell divisions leads to a virtually invariant division pattern, including those that create new tissue layers. However, the mechanisms that control oriented cell divisions are hitherto poorly understood. Here, we reveal one such mechanism in which FEZ and SOMBRERO (SMB), two plant-specific NAC-domain transcription factors, control the delicately tuned reorientation and timing of cell division in a subset of stem cells. FEZ is expressed in root cap stem cells, where it promotes periclinal, root cap-forming cell divisions. In contrast, SMB negatively regulates FEZ activity, repressing stem cell-like divisions in the root cap daughter cells. FEZ becomes expressed in predivision stem cells, induces oriented cell division, and activates expression of its negative regulator, SMB, thus generating a feedback loop for controlled switches in cell division plane.
Developmental cell 01/2009; 15(6):913-22. · 13.36 Impact Factor
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Pankaj Dhonukshe,
Hirokazu Tanaka,
Tatsuaki Goh,
Kazuo Ebine,
Ari Pekka Mähönen,
Kalika Prasad,
Ikram Blilou,
Niko Geldner, Jian Xu,
Tomohiro Uemura,
Joanne Chory,
Takashi Ueda,
Akihiko Nakano,
Ben Scheres,
Jirí Friml
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ABSTRACT: Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication-a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.
Nature 11/2008; 456(7224):962-6. · 36.28 Impact Factor
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Pankaj Dhonukshe,
Hirokazu Tanaka,
Tatsuaki Goh,
Kazuo Ebine,
Ari Pekka M|[auml]|h|[ouml]|nen,
Kalika Prasad,
Ikram Blilou,
Niko Geldner, Jian Xu,
Tomohiro Uemura,
Joanne Chory,
Takashi Ueda,
Akihiko Nakano,
Ben Scheres,
Ji|[rcaron]||[iacute]| Friml
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ABSTRACT: Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication—a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family
Nature 10/2008; 456(7224):962-966. · 36.28 Impact Factor
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ABSTRACT: The plant growth regulator auxin controls cell identity, cell division and cell expansion. Auxin efflux facilitators (PINs) are associated with auxin maxima in distal regions of both shoots and roots. Here we model diffusion and PIN-facilitated auxin transport in and across cells within a structured root layout. In our model, the stable accumulation of auxin in a distal maximum emerges from the auxin flux pattern. We have experimentally tested model predictions of robustness and self-organization. Our model explains pattern formation and morphogenesis at timescales from seconds to weeks, and can be understood by conceptualizing the root as an 'auxin capacitor'. A robust auxin gradient associated with the maximum, in combination with separable roles of auxin in cell division and cell expansion, is able to explain the formation, maintenance and growth of sharply bounded meristematic and elongation zones. Directional permeability and diffusion can fully account for stable auxin maxima and gradients that can instruct morphogenesis.
Nature 11/2007; 449(7165):1008-13. · 36.28 Impact Factor
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ABSTRACT: The plant growth regulator auxin controls cell identity, cell division and cell expansion. Auxin efflux facilitators (PINs) are associated with auxin maxima in distal regions of both shoots and roots. Here we model diffusion and PIN-facilitated auxin transport in and across cells within a structured root layout. In our model, the stable accumulation of auxin in a distal maximum emerges from the auxin flux pattern. We have experimentally tested model predictions of robustness and self-organization. Our model explains pattern formation and morphogenesis at timescales from seconds to weeks, and can be understood by conceptualizing the root as an 'auxin capacitor'. A robust auxin gradient associated with the maximum, in combination with separable roles of auxin in cell division and cell expansion, is able to explain the formation, maintenance and growth of sharply bounded meristematic and elongation zones. Directional permeability and diffusion can fully account for stable auxin maxima and gradients that can instruct morphogenesis.
Nature 10/2007; 449(7165):1008-1013. · 36.28 Impact Factor
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ABSTRACT: Polar flow of the phytohormone auxin requires plasma membrane-associated PIN proteins and underlies multiple developmental processes in plants. Here we address the importance of the polarity of subcellular PIN localization for the directionality of auxin transport in Arabidopsis thaliana. Expression of different PINs in the root epidermis revealed the importance of PIN polar positions for directional auxin flow and root gravitropic growth. Interfering with sequence-embedded polarity signals directly demonstrates that PIN polarity is a primary factor in determining the direction of auxin flow in meristematic tissues. This finding provides a crucial piece in the puzzle of how auxin flow can be redirected via rapid changes in PIN polarity.
Science 06/2006; 312(5775):883. · 31.20 Impact Factor
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Genes & Development 05/2006; 20(8):922-6. · 11.66 Impact Factor
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ABSTRACT: Plants and some animals have a profound capacity to regenerate organs from adult tissues. Molecular mechanisms for regeneration have, however, been largely unexplored. Here we investigate a local regeneration response in Arabidopsis roots. Laser-induced wounding disrupts the flow of auxin-a cell-fate-instructive plant hormone-in root tips, and we demonstrate that resulting cell-fate changes require the PLETHORA, SHORTROOT, and SCARECROW transcription factors. These transcription factors regulate the expression and polar position of PIN auxin efflux-facilitating membrane proteins to reconstitute auxin transport in renewed root tips. Thus, a regeneration mechanism using embryonic root stem-cell patterning factors first responds to and subsequently stabilizes a new hormone distribution.
Science 02/2006; 311(5759):385-8. · 31.20 Impact Factor
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ABSTRACT: Cell polarity plays an important role in plant development, but the mechanisms that first establish polarity cues remain obscure. By contrast, a flurry of information has recently emerged on the elaboration of cell shape from such unknown initial cell-polarity cues. Recent studies suggest that Rho-related GTPases in plants (ROPs), and their effector targets among the ROP-interactive CRIB motif-containing proteins (RICs), mediate two antagonistic pathways that have opposing action on cell polarization. ROP proteins appear to interact directly with upstream regulators of the ARP2/3 complex, which are conserved modulators of the actin cytoskeleton. ROP function is dependent on the class 1 ADP-ribosylation factors (ARFs), which are core components of the vesicle transport machinery that are also involved in the polar localization of PIN-FORMED (PIN) family auxin efflux facilitators.
Current Opinion in Plant Biology 01/2006; 8(6):613-8. · 9.27 Impact Factor
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ABSTRACT: CLAVATA3 (CLV3), CLV3/ESR19 (CLE19), and CLE40 belong to a family of 26 genes in Arabidopsis thaliana that encode putative peptide ligands with unknown identity. It has been shown previously that ectopic expression of any of these three genes leads to a consumption of the root meristem. Here, we show that in vitro application of synthetic 14-amino acid peptides, CLV3p, CLE19p, and CLE40p, corresponding to the conserved CLE motif, mimics the overexpression phenotype. The same result was observed when CLE19 protein was applied externally. Interestingly, clv2 failed to respond to the peptide treatment, suggesting that CLV2 is involved in the CLE peptide signaling. Crossing of the CLE19 overexpression line with clv mutants confirms the involvement of CLV2. Analyses using tissue-specific marker lines revealed that the peptide treatments led to a premature differentiation of the ground tissue daughter cells and misspecification of cell identity in the pericycle and endodermis layers. We propose that these 14-amino acid peptides represent the major active domain of the corresponding CLE proteins, which interact with or saturate an unknown cell identity-maintaining CLV2 receptor complex in roots, leading to consumption of the root meristem.
The Plant Cell 10/2005; 17(9):2542-53. · 8.99 Impact Factor
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ABSTRACT: Vesicle trafficking is essential for the generation of asymmetries, which are central to multicellular development. Core components of the vesicle transport machinery, such as ADP-ribosylation factor (ARF) GTPases, have been studied primarily at the single-cell level. Here, we analyze developmental functions of the ARF1 subclass of the Arabidopsis thaliana multigene ARF family. Six virtually identical ARF1 genes are ubiquitously expressed, and single loss-of-function mutants in these genes reveal no obvious developmental phenotypes. Fluorescence colocalization studies reveal that ARF1 is localized to the Golgi apparatus and endocytic organelles in both onion (Allium cepa) and Arabidopsis cells. Apical-basal polarity of epidermal cells, reflected by the position of root hair outgrowth, is affected when ARF1 mutants are expressed at early stages of cell differentiation but after they exit mitosis. Genetic interactions during root hair tip growth and localization suggest that the ROP2 protein is a target of ARF1 action, but its localization is slowly affected upon ARF1 manipulation when compared with that of Golgi and endocytic markers. Localization of a second potential target of ARF1 action, PIN2, is also affected with slow kinetics. Although extreme redundancy precludes conventional genetic dissection of ARF1 functions, our approach separates different ARF1 downstream networks involved in local and specific aspects of cell polarity.
The Plant Cell 03/2005; 17(2):525-36. · 8.99 Impact Factor
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ABSTRACT: Local accumulation of the plant growth regulator auxin mediates pattern formation in Arabidopsis roots and influences outgrowth and development of lateral root- and shoot-derived primordia. However, it has remained unclear how auxin can simultaneously regulate patterning and organ outgrowth and how its distribution is stabilized in a primordium-specific manner. Here we show that five PIN genes collectively control auxin distribution to regulate cell division and cell expansion in the primary root. Furthermore, the joint action of these genes has an important role in pattern formation by focusing the auxin maximum and restricting the expression domain of PLETHORA (PLT) genes, major determinants for root stem cell specification. In turn, PLT genes are required for PIN gene transcription to stabilize the auxin maximum at the distal root tip. Our data reveal an interaction network of auxin transport facilitators and root fate determinants that control patterning and growth of the root primordium.
Nature 01/2005; 433(7021):39-44. · 36.28 Impact Factor
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ABSTRACT: In the Arabidopsis shoot apical meristem, an organizing center signals in a non-cell-autonomous manner to specify the overlying stem cells. Stem cells express the small, secreted protein CLAVATA3 (CLV3; ) that activates the CLV1-CLV2 receptor complex, which negatively controls the size of the organizing center. Consistently, CLV3 overexpression restricts shoot meristem size. The root meristem also contains a stem cell organizer, and here we show that localized overexpression in roots of CLE19, encoding a CLV3 homolog, restricts the size of the root meristem. This suggests that CLE19 acts by overactivating an endogenous CLV-like pathway involved in root meristem maintenance. Surprisingly, CLE19 restricts meristem size without directly interfering with organizer and stem cell specification. We isolated mutations in two loci, SOL1 and SOL2, which suppress the CLE19 overexpression phenotype. sol2 plants display floral phenotypes reminiscent of clv weak alleles; these phenotypes suggest that components of a CLV pathway are shared in roots and shoots. SOL1 encodes a putative Zn(2+)-carboxypeptidase, which may be involved in ligand processing.
Current Biology 09/2003; 13(16):1435-41. · 9.65 Impact Factor
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ABSTRACT: In contrast to the intense attention devoted to research on intracellular sterol trafficking in animal cells, knowledge about sterol transport in plant cells remains limited, and virtually nothing is known about plant endocytic sterol trafficking. Similar to animals, biosynthetic sterol transport occurs from the endoplasmic reticulum (ER) via the Golgi apparatus to the plasma membrane. The vesicle trafficking inhibitor brefeldin A (BFA) has been suggested to disrupt biosynthetic sterol transport at the Golgi level.
Here, we report on early endocytic sterol trafficking in Arabidopsis root epidermal cells by introducing filipin as a tool for fluorescent sterol detection. Sterols can be internalized from the plasma membrane and localize to endosomes positive for the early endosomal Rab5 GTPase homolog ARA6 fused to green fluorescent protein (GFP) (ARA6-GFP). Early endocytic sterol transport is actin dependent and highly BFA sensitive. BFA causes coaccumulation of sterols, endocytic markers like ARA6-GFP, and PIN2, a polarly localized presumptive auxin transport protein, in early endosome agglomerations that can be distinguished from ER and Golgi. Sterol accumulation in such aggregates is enhanced in actin2 mutants, and the actin-depolymerizing drug cytochalasin D inhibits sterol redistribution from endosome aggregations.
Early endocytic sterol trafficking involves transport via ARA6-positive early endosomes that, in contrast to animal cells, is actin dependent. Our results reveal sterol-enriched early endosomes as targets for BFA interference in plants. Early endocytic sterol trafficking and recycling of polar PIN2 protein share a common pathway, suggesting a connection between plant endocytic sterol transport and polar sorting events.
Current Biology 09/2003; 13(16):1378-87. · 9.65 Impact Factor
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ABSTRACT: Local accumulation of the plant growth regulator auxin mediates pattern formation in Arabidopsis roots and influences outgrowth and development of lateral root-and shoot-derived primordia. However, it has remained unclear how auxin can simultaneously regulate patterning and organ outgrowth and how its distribution is stabilized in a primordium-specific manner. Here we show that five PIN genes collectively control auxin distribution to regulate cell division and cell expansion in the primary root. Furthermore, the joint action of these genes has an important role in pattern formation by focusing the auxin maximum and restricting the expression domain of PLETHORA (PLT) genes, major determinants for root stem cell specification. In turn, PLT genes are required for PIN gene transcription to stabilize the auxin maximum at the distal root tip. Our data reveal an interaction network of auxin transport facilitators and root fate determinants that control patterning and growth of the root primordium. In Arabidopsis root development, a distal auxin maximum corre-lates with pattern formation and the orientation and extent of cell division 1 . Inhibition of polar auxin transport strongly affects these processes 1 . The initiation of lateral roots and leaf primordia is also associated with changes in auxin transport 2–4 . These observations point to polar auxin transport as a major factor in organ formation. Recent analyses of the Arabidopsis PIN proteins revealed their association with auxin maxima in distal domains of organ primor-dia 2–4 . The PIN genes are thought to encode components of the auxin efflux machinery mediating polar auxin transport, as con-cluded from the polar localization of PIN membrane proteins and auxin uptake experiments 5–11 . PIN proteins might participate directly in auxin transport or help in the assembly of other proteins with efflux activity such as the AtMDR/PGP proteins 12,13 . Mutations in the ARF-GEF GNOM, required for vesicle transport of PIN1, also lead to developmental defects that resemble those caused by interfering with auxin transport 14–16 . All single pin mutants described so far display different weak phenotypes in primary roots 4–8 , in contrast with gnom mutants and polar auxin transport inhibitor treatments. Here, we investigate the collective contribution of five PIN genes in the control of cell division and cell expansion during root outgrowth. Further-more, we assess how the PLETHORA (PLT) genes, which encode auxin-inducible AP2-domain putative transcription factors necess-ary and sufficient for stem cell specification in the root primor-dium 17 , respond to and regulate PIN gene activity during pattern formation.
