The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in<i>Arabidopsis thaliana</i>

Zourelidou, Melina; Müller, Isabel; Willige, Björn C.; Nill, Carola; Jikumaru, Yusuke; Li, Hanbing; Schwechheimer, Claus

doi:10.1242/dev.028365

Cited by 147 publications

(215 citation statements)

References 59 publications

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“…We found that PIN1 phosphorylation was not detectably impaired in complex mutants of the D6PK and PIDrelated kinases, suggesting that other protein kinases (e.g., other protein kinases of the AGCVIII family) also regulate PIN phosphorylation in addition to D6PKs and PID/WAGs. This hypothesis finds indirect support in the observation that root growth and gravitropism are not as severely impaired in the complex d6pk or pid/wag mutants as may be expected from mutants with severely impaired PIN and auxin transport function (10,17,20,31,35). Several of the phosphorylation events observed in our experiments support the notion that these, as yet, unknown PIN1-regulatory protein kinases are related-in their cell biological behavior-to D6PK and PID.…”

Section: Pin1 Phosphorylation Can Be Detected At the Basal Domains Insupporting

confidence: 61%

“…as with decreases in directional auxin transport in stems and hypocotyls (13,16,17). Thus, PIN1 phosphorylation is essential for auxin transport in planta and may allow predicting PIN1 activity in situ.…”

Section: Significancementioning

confidence: 99%

“…Genetic studies indicate that D6PK acts in a functionally redundant manner with at least three other sequence-related D6PK-LIKE genes (12,16,17). Based on genetic and cell biological studies, functional redundancy was also proposed between PID, WAG1, and WAG2, and possibly with PID2, which are all members of a distinct subclade within the Arabidopsis AGCVIII protein kinase family (30,31).…”

Section: Pin1 Phosphorylation Can Be Detected At the Basal Domains Inmentioning

confidence: 99%

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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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Section: Pin1 Phosphorylation Can Be Detected At the Basal Domains Insupporting

confidence: 61%

Section: Significancementioning

confidence: 99%

Section: Pin1 Phosphorylation Can Be Detected At the Basal Domains Inmentioning

confidence: 99%

See 1 more Smart Citation

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 polar PIN localization determines direction of the auxin flow; thus, any signal that acts upstream to control the cellular PIN localization and activity can be translated into changes in the auxin distribution that modulate multiple aspects of the plant development. Phosphorylation has been shown to be important for auxin transport and distribution (17)(18)(19)(20). So far, the only known regulators that specifically regulate the PIN polar targeting are the serine/threonine protein kinase PINOID (PID) (18-20) and the protein phosphatase 2A (PP2A) (21, 22) that mediate antagonistically the phosphorylation of PIN proteins (22).…”

mentioning

confidence: 99%

PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport

Zhang

Nodzyński

Pěnčík

et al. 2009

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

181

171

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The plant hormone auxin plays a crucial role in regulating plant development and plant architecture. The directional auxin distribution within tissues depends on PIN transporters that are polarly localized on the plasma membrane. The PIN polarity and the resulting auxin flow directionality are mediated by the antagonistic actions of PINOID kinase and protein phosphatase 2A. However, the contribution of the PIN phosphorylation to the polar PIN sorting is still unclear. Here, we identified an evolutionarily conserved phosphorylation site within the central hydrophilic loop of PIN proteins that is important for the apical and basal polar PIN localizations. Inactivation of the phosphorylation site in PIN1(Ala) resulted in a predominantly basal targeting and increased the auxin flow to the root tip. In contrast, the outcome of the phosphomimic PIN1(Asp) manipulation was a constitutive, PINOID-independent apical targeting of PIN1 and an increased auxin flow in the opposite direction. Furthermore, the PIN1(Asp) functionally replaced PIN2 in its endogenous expression domain, revealing that the phosphorylation-dependent polarity regulation contributes to functional diversification within the PIN family. Our data suggest that PINOID-independent PIN phosphorylation at one single site is adequate to change the PIN polarity and, consequently, to redirect auxin fluxes between cells and provide the conceptual possibility and means to manipulate auxin-dependent plant development and architecture.cell polarity | auxin distribution | plant architecture T he plant hormone auxin acts, on account of its differential distribution (gradients) within tissues, as a major determinant of plant architecture (1-3). Auxin is distributed throughout the plant by a network of carrier proteins (4-8), and the directionality of the auxin flow is determined by asymmetrically localized plasma membrane PIN transporters (9). The differentially expressed and polarly localized PIN proteins constitute the backbone of a transport network for directional auxin distribution in different parts of the plant (10). The local biosynthesis (11-13) together with the PIN-dependent transport (14) largely account for the formation of local auxin maxima and minima that regulate various developmental processes, including embryonic axis establishment, tropic growth, root meristem patterning, lateral organ and fruit formation, and vascular tissue differentiation and regeneration (15, 16). The polar PIN localization determines direction of the auxin flow; thus, any signal that acts upstream to control the cellular PIN localization and activity can be translated into changes in the auxin distribution that modulate multiple aspects of the plant development. Phosphorylation has been shown to be important for auxin transport and distribution (17)(18)(19)(20). So far, the only known regulators that specifically regulate the PIN polar targeting are the serine/threonine protein kinase PINOID (PID) (18-20) and the protein phosphatase 2A (PP2A) (21, 22) that mediate antagonistical...

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“…Interestingly, although loss of phototropin 1 (the blue light receptor belonging to the AGC2 subgroup) impaired PIN3 polarization in the hypocotyl endodermis, it did not directly phosphorylate the PIN3 hydrophilic loop in vitro (Ding et al, 2011). Zourelidou et al (2009) reported that D6PK (D6 protein kinase), another AGC1 subgroup protein kinase, might be implicated in auxin transport, most likely by modulating PIN activity. D6PK was able to phosphorylate the hydrophilic loop of several PINs in vitro and in Arabidopsis protoplasts.…”

Section: Agc1 Kinases Directly Phosphorylate the Pin Hydrophilic Loopmentioning

confidence: 99%

Regulation of the Polarity of Protein Trafficking by Phosphorylation

Ganguly

Sasayama

Cho

2012

Molecules and Cells

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The asymmetry of environmental stimuli and the execution of developmental programs at the organism level require a corresponding polarity at the cellular level, in both unicellular and multicellular organisms. In plants, cell polarity is important in major developmental processes such as cell division, cell enlargement, cell morphogenesis, embryogenesis, axis formation, organ development, and defense. One of the most important factors controlling cell polarity is the asymmetric distribution of polarity determinants. In particular, phosphorylation is implicated in the polar distribution of the determinant protein factors, a mechanism conserved in both prokaryotes and eukaryotes. In plants, formation of local gradients of auxin, the morphogenic hormone, is critical for plant developmental processes exhibiting polarity. The auxin efflux carriers PIN-FORMEDs (PINs) localize asymmetrically in the plasma membrane and cause the formation of local auxin gradients throughout the plant. The asymmetry of PIN distribution in the plasma membrane is determined by phosphorylationmediated polar trafficking of PIN proteins. This review discusses recent studies on the role of phosphorylation in polar PIN trafficking.

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The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport inArabidopsis thaliana

Cited by 147 publications

References 59 publications

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

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

PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport

Regulation of the Polarity of Protein Trafficking by Phosphorylation

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