Phosphoinositide Signaling in Root Hair Tip Growth

Kusano, Hiroaki; Tominaga, Rumi; Wada, Takuji; Kato, Mariko; Aoyama, Takashi

doi:10.1002/9781118647363.ch9

Cited by 3 publications

(5 citation statements)

References 185 publications

(209 reference statements)

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“…These steps of RH growth and development are tightly regulated by numerous genes, encoding transcription factors (TFs), and proteins involved in cell wall remodeling, cytoskeletal dynamics and vesicle trafficking. Furthermore, hormones such as auxin, ethylene, jasmonic acid or cytokinin and other signaling molecules including reactive oxygen species (ROS), cytoplasmic calcium ion (Ca 2+ ) and phosphoinositides play pivotal roles in modulating RH development (Pitts et al ., 1998 ; Kusano et al ., 2014 ; Mendrinna & Persson, 2015 ; Mangano et al ., 2017 ; Kato et al ., 2019 ; Han et al ., 2020 ; Tian et al ., 2020 ; Wendrich et al ., 2020 ).…”

Section: Introductionmentioning

confidence: 99%

A phosphorus‐limitation induced, functionally conserved DUF506 protein is a repressor of root hair elongation in plants

et al. 2021

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Root hairs (RHs) function in nutrient and water acquisition, root metabolite exudation, soil anchorage and plant-microbe interactions. Longer or more abundant RHs are potential breeding traits for developing crops that are more resource-use efficient and can improve soil health.While many genes are known to promote RH elongation, relatively little is known about genes and mechanisms that constrain RH growth.Here we demonstrate that a DOMAIN OF UNKNOWN FUNCTION 506 (DUF506) protein, AT3G25240, negatively regulates Arabidopsis thaliana RH growth. The AT3G25240 gene is strongly and specifically induced during phosphorus (P)-limitation. Mutants of this gene, which we call REPRESSOR OF EXCESSIVE ROOT HAIR ELONGATION 1 (RXR1), have much longer RHs, higher phosphate content and seedling biomass, while overexpression of the gene exhibits opposite phenotypes. Co-immunoprecipitation, pull-down and bimolecular fluorescence complementation (BiFC) analyses reveal that RXR1 physically interacts with a RabD2c GTPase in nucleus, and a rabd2c mutant phenocopies the rxr1 mutant. Furthermore, N-terminal variable region of RXR1 is crucial for inhibiting RH growth. Overexpression of a Brachypodium distachyon RXR1 homolog results in repression of RH elongation in Brachypodium.Taken together, our results reveal a novel DUF506-GTPase module with a prominent role in repression of plant RH elongation especially under P stress.

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Section: Introductionmentioning

confidence: 99%

A phosphorus‐limitation induced, functionally conserved DUF506 protein is a repressor of root hair elongation in plants

et al. 2021

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“…8), therefore may limit beta-oxidation (Fulda et al, 2002; Shockey et al, 2002)and thus energy production required for RH elongation growth. On the other hand, interaction with LACS4 could indicate that some other aspect of RH lipid metabolism, such as the provision of activated fatty acids for membrane lipid or phosphoinositide synthesis, is controlled by RXR1/RXR2.During RH tip growth, membrane lipids are required in large amounts for the expanding plasma membrane, while phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) is a key signaling molecule in the process(Stenzel et al, 2008; Kato et al, 2013; Kusano et al, 2014; Kato et al, 2019) Despite the absence of mutant RH phenotypes, the aforementioned RXR1-interacting proteins At1g12000 (β-subunit of pyrophosphate-dependent phosphofructokinase; PPi- PFK) and At1g78850 (mannose-binding lectin1) are intriguing. PPi-PFK is a key enzyme that facilitates glycolytic flux during severe Pi stress when the intracellular levels of adenylates and Pi are very low (Plaxton and Tran, 2011), whereas At1g78850 enhances purple acid phosphatase 26 (PAP26) function to facilitate Pi-scavenging by Pi-starved plants (Ghahremani et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…These steps of RH growth and development are tightly regulated by numerous genes, encoding transcription factors (TFs), and proteins involved in cell wall remodeling, cytoskeletal dynamics and vesicle trafficking. Furthermore, hormones such as auxin, ethylene, jasmonic acid or cytokinin and other signaling molecules including reactive oxygen species (ROS), cytoplasmic Ca 2+ and phosphoinositides play pivotal roles in modulating RH development (Pitts et al, 1998; Kusano et al, 2014; Mendrinna and Persson, 2015; Mangano et al, 2017; Kato et al, 2019; Han et al, 2020; Tian et al, 2020; Wendrich et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

A Phosphorus-Limitation Induced, Functionally Conserved DUF506 Protein is a Repressor of Root Hair Elongation in Arabidopsis thaliana

Ying

Blancaflor

Liao³

et al. 2021

Preprint

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Root hairs (RHs) function in nutrient and water acquisition, root metabolite exudation, soil anchorage and plant-microbe interactions. Longer or more abundant RHs are potential breeding traits for developing crops that are more resource-use efficient and can improve soil health. RH elongation is controlled by both environmental and endogenous factors. While many genes are known to promote RH elongation, relatively little is known about genes and mechanisms that constrain RH growth. Here we demonstrate that a DOMAIN OF UNKNOWN FUNCTION 506 (DUF506) protein, AT3G25240, negatively regulates Arabidopsis thaliana RH growth. The AT3G25240 gene is strongly and specifically induced during P-limitation. Mutants of this gene, which we call REPRESSOR OF EXCESSIVE ROOT HAIR ELONGATION 1 (RXR1), have much longer RHs, while over-expression of the gene results in much shorter RHs. RXR1 physically interacts with a Rab-GTPase (RXR2), and an rxr2 mutant phenocopies the rxr1 mutant. Overexpression of a Brachypodium distachyon RXR1 homolog resulted in repression of RH elongation in Brachypodium. Taken together, our results reveal a DUF506-GTPase module with a prominent role in repression of RH elongation that is conserved in monocots and dicots.

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“…These features of PtdIns(4,5)P 2 have been revealed primarily in animal studies, and are generally applicable to plants (Munnik and Nielsen, ; Gerth et al ., ). In recent years, the PtdIns(4,5)P 2 signal has been studied intensively in plants, especially for its involvement in root hair and pollen tube growth (Kusano et al ., ; Sekereš et al ., ; Heilmann and Ischebeck, ).…”

Section: Introductionmentioning

confidence: 99%

“…In the subapical plasma membrane, clathrin-mediated endocytosis occurs (Emons and Traas, 1986;Galway et al, 1997) for membrane recycling to the apical plasma membrane (Hepler et al, 2001;Samaj et al, 2005). The polarity of tip growth is assumed to be established and maintained through a robust mechanism involving calcium ions (Ca 2+ ), reactive oxygen species (ROS), Rho-family GTPases of plants (ROPs), and PtdIns(4,5) P 2 (Kusano et al, 2014;Smith and Oppenheimer, 2005;Cole and Fowler, 2006;Lee and Yang, 2008;C ardenas, 2009). In Arabidopsis root hair cells, fluorescent protein fusions of ROP2, ROP4, and ROP6 localized preferentially to the plasma membrane at the future bulge-formation site and the elongating tip region (Molendijk et al, 2001;Jones et al, 2002), where the ROP signal stimulates a positive regulatory loop involving ROS and Ca 2+ signals via the NADPH oxidase ROOT HAIR DEFECTIVE 2 (Foreman et al, 2003;Jones et al, 2007;Takeda et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5‐bisphosphate signal on the plasma membrane and attenuates root hair elongation

et al. 2019

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Summary Phosphatidylinositol 4,5‐bisphosphate [PtdIns(4,5)P2] serves as a subcellular signal on the plasma membrane, mediating various cell‐polarized phenomena including polar cell growth. Here, we investigated the involvement of Arabidopsis thaliana PCaP2, a plant‐unique plasma membrane protein with phosphoinositide‐binding activity, in PtdIns(4,5)P2 signaling for root hair tip growth. The long‐root‐hair phenotype of the pcap2 knockdown mutant was found to stem from its higher average root hair elongation rate compared with the wild type and to counteract the low average rate caused by a defect in the PtdIns(4,5)P2‐producing enzyme gene PIP5K3. On the plasma membrane of elongating root hairs, the PCaP2 promoter‐driven PCaP2–green fluorescent protein (GFP), which complemented the pcap2 mutant phenotype, overlapped with the PtdIns(4,5)P2 marker 2xCHERRY‐2xPHPLC in the subapical region, but not at the apex, suggesting that PCaP2 attenuates root hair elongation via PtdIns(4,5)P2 signaling on the subapical plasma membrane. Consistent with this, a GFP fusion with the PCaP2 phosphoinositide‐binding domain PCaP2N23, root hair‐specific overexpression of which caused a low average root hair elongation rate, localized more intense to the subapical plasma membrane than to the apical plasma membrane similar to PCaP2–GFP. Inducibly overexpressed PCaP2–GFP, but not its derivative lacking the PCaP2N23 domain, replaced 2xCHERRY‐2xPHPLC on the plasma membrane in root meristematic epidermal cells, and suppressed FM4‐64 internalization in elongating root hairs. Moreover, inducibly overexpressed PCaP2 arrested an endocytic process of PIN2–GFP recycling. Based on these results, we conclude that PCaP2 functions as a negative modulator of PtdIns(4,5)P2 signaling on the subapical plasma membrane probably through competitive binding to PtdIns(4,5)P2 and attenuates root hair elongation.

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Phosphoinositide Signaling in Root Hair Tip Growth

Cited by 3 publications

References 185 publications

A phosphorus‐limitation induced, functionally conserved DUF506 protein is a repressor of root hair elongation in plants

A phosphorus‐limitation induced, functionally conserved DUF506 protein is a repressor of root hair elongation in plants

A Phosphorus-Limitation Induced, Functionally Conserved DUF506 Protein is a Repressor of Root Hair Elongation in Arabidopsis thaliana

Arabidopsis PCaP2 modulates the phosphatidylinositol 4,5‐bisphosphate signal on the plasma membrane and attenuates root hair elongation

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