Molecular Mechanisms Regulating Root Hair Tip Growth: A Comparison with Pollen Tubes

Schoenaers, Sébastjen; Balcerowicz, Daria; Vissenberg, Kris

doi:10.1007/978-3-319-56645-0_9

Cited by 24 publications

(26 citation statements)

References 422 publications

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“…A similar expression pattern where a plasma membrane proton pump was excluded from the growing pollen tube tip has been described in tobacco (Certal et al 2008). The fact that AHA7 is present in the tip of growing root hair cells but excluded from the tip of growing pollen tubes suggests that tip growth in root hairs and pollen tubes underlies different molecular programs, as hypothesized before (Schoenaers et al ), and indicates that AHA7 plays different roles in these two programs.…”

Section: Resultsmentioning

confidence: 51%

Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana

Hoffmann

Olsen

Ezike

et al. 2018

Physiologia Plantarum

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Plasma membrane H+‐ATPase pumps build up the electrochemical H+ gradients that energize most other transport processes into and out of plant cells through channel proteins and secondary active carriers. In Arabidopsis thaliana, the AUTOINHIBITED PLASMA MEMBRANE H+‐ATPases AHA1, AHA2 and AHA7 are predominant in root epidermal cells. In contrast to other H+‐ATPases, we find that AHA7 is autoinhibited by a sequence present in the extracellular loop between transmembrane segments 7 and 8. Autoinhibition of pump activity was regulated by extracellular pH, suggesting negative feedback regulation of AHA7 during establishment of an H+ gradient. Due to genetic redundancy, it has proven difficult to test the role of AHA2 and AHA7, and mutant phenotypes have previously only been observed under nutrient stress conditions. Here, we investigated root and root hair growth under normal conditions in single and double mutants of AHA2 and AHA7. We find that AHA2 drives root cell expansion during growth but that, unexpectedly, restriction of root hair elongation is dependent on AHA2 and AHA7, with each having different roles in this process.

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Section: Resultsmentioning

confidence: 51%

Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana

Hoffmann

Olsen

Ezike

et al. 2018

Physiologia Plantarum

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“…This relatively subtle growth phenotype stands in stark contrast to the eru RH phenotype. However, despite that fact that we do not know what is causing the eru PT growth defect, and the similarities between PT and RH tip growth, important differences between both apical growth regimes exist and could relate to the observed phenotypic difference ( Schoenaers et al, 2017 ). To better understand the mechanism(s) related to affected eru PT growth we studied [Ca 2+ ] cyt dynamics under different [Ca 2+ ] ext .…”

Section: Discussionmentioning

confidence: 97%

“…The PT and RH tip growth pathways likely share multiple regulatory components ( Schiefelbein et al, 1993 ; Procissi et al, 2003 ; Becker et al, 2014 ; Schoenaers et al, 2017 ). The CrRLK1L family protein ERULUS was shown to have a crucial role in regulating RH morphogenesis in Arabidopsis thaliana ( Bai et al, 2014a ; Haruta et al, 2014 ).…”

Section: Discussionmentioning

confidence: 99%

“…More so, Ca 2+ -signatures seem embedded throughout the male–female tissue crosstalk pathway ( Denninger et al, 2014 ; Hamamura et al, 2014 ). A number of highly dynamic cellular processes occur during PT growth ( Obermeyer and Feijó, 2017 ), including the formation and maintenance of intra- and extracellular ion dynamics, apical endo-/exocytosis and the modification of the cytoskeleton, all of which depend on tight spatial and temporal control of cytosolic [Ca 2+ ] oscillations at the tip ( Schoenaers et al, 2017 ). Pharmacological interruption of the apical cytoplasmic Ca 2+ gradient causes immediate growth cessation ( Iwano et al, 2009 ), and local elevation of the [Ca 2+ ] ext irreversibly steers tip growth directionality in vitro ( Bibikova et al, 1997 ).…”

Section: Introductionmentioning

confidence: 99%

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The Kinase ERULUS Controls Pollen Tube Targeting and Growth in Arabidopsis thaliana

et al. 2017

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In this paper, we describe the role of the receptor-like kinase ERULUS (ERU) in PT growth of Arabidopsis thaliana. In silico analysis and transcriptional reporter lines revealed that ERU is only expressed in pollen and root hairs (RHs), making it a tip growth-specific kinase. Deviations from Mendelian inheritance were observed in the offspring of self-pollinated heterozygous eru plants. We found that in vivo eru PT targeting was disturbed, providing a possible explanation for the observed decrease in eru fertilization competitiveness. Extracellular calcium perception and intracellular calcium dynamics lie at the basis of in vivo pollen tube (PT) tip growth and guidance. In vitro, ERU loss-of-function lines displayed no obvious PT phenotype, unless grown on low extracellular calcium ([Ca2+]ext) medium. When grown at 12 the normal [Ca2+]ext, eru PTs grew 37% slower relative to WT PTs. Visualization of cytoplasmic [Ca2+]cyt oscillations using the Yellow Cameleon 3.6 (YC3.6) calcium sensor showed that, unlike in WT PTs, eru apical [Ca2+]cyt oscillations occur at a lower frequency when grown at lower [Ca2+]ext, consistent with the observed reduced growth velocity. Our results show that the tip growth-specific kinase ERULUS is involved in regulating Ca2+-dependent PT growth, and most importantly, fertilization efficiency through successful PT targeting to the ovules.

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“…Root hairs (RHs) are non‐essential protuberances of the root epidermis that facilitate uptake of water and nutrients as well as anchoring in the soil . The polarized tip growth of RHs is brought about by a complex interplay of hormones, second messengers, and pH homeostasis . Recent studies supported a crucial role of auxin uptake and signaling in regulating Cyclic Nucleotide–Gated ion Channels (CNGCs) and Receptor‐Like Kinase (RLK) function for controlling Ca 2+ signaling and cell wall composition during tip growth .…”

mentioning

confidence: 99%

CBL1‐CIPK26‐mediated phosphorylation enhances activity of the NADPH oxidase RBOHC, but is dispensable for root hair growth

et al. 2018

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Root hairs (RH) are tip growing polarized cells aiding the uptake of nutrients and water into plants. RH differentiation involves the interplay of various hormones and second messengers. Tightly regulated production of reactive oxygen species by the NADPH oxidase RBOHC crucially functions in RH differentiation and Ca -dependent phosphorylation has been implemented in these processes. However, the kinases regulating RBOHC remained enigmatic. Here we identify CBL1-CIPK26 Ca sensor-kinase complexes as modulators of RBOHC activity. Combined genetic, cell biological and biochemical analyses reveal synergistic function of CIPK26-mediated phosphorylation and Ca binding for RBOHC activation. Complementation of rbohC mutant RH phenotypes by a S318/322 phosphorylation deficient RBOHC version suggests flexible and alternating phosphorylation patterns as mechanism fine-tuning ROS production in RH development.

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Molecular Mechanisms Regulating Root Hair Tip Growth: A Comparison with Pollen Tubes

Cited by 24 publications

References 422 publications

Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana

Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana

The Kinase ERULUS Controls Pollen Tube Targeting and Growth in Arabidopsis thaliana

CBL1‐CIPK26‐mediated phosphorylation enhances activity of the NADPH oxidase RBOHC, but is dispensable for root hair growth

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