Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity

Hwang, Jae‐Ung; Wu, Gwo-Jang; An, Yan; Lee, Yong-Jik; Grierson, Claire; Yang, Zhenbiao

doi:10.1242/jcs.039180

Cited by 81 publications

(113 citation statements)

References 45 publications

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“…Various regulators that modulate the shuttling between inactive and active forms of ROP GTPases have been identified, including guanine nucleotide exchange factors (RopGEFs) that stimulate GDP-to-GTP exchange to activate ROP GTPases, ROP GTPase-activating proteins (RopGAPs) that accelerate GTP hydrolysis, and guanine nucleotide dissociation inhibitors (RhoGDIs) that inhibit GDP release, thus shifting ROP GTPases toward the inactive state. Some of these regulators have been shown to modulate ROP GTPase activity in pollen tubes and root hairs (Carol et al, 2005;Gu et al, 2006;Zhang and McCormick, 2007;Hwang et al, 2008Hwang et al, , 2010Riely et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Lei

Wang

et al. 2015

Plant Cell

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Rhizobia preferentially enter legume root hairs via infection threads, after which root hairs undergo tip swelling, branching, and curling. However, the mechanisms underlying such root hair deformation are poorly understood. Here, we showed that a type II small GTPase, ROP10, of Medicago truncatula is localized at the plasma membrane (PM) of root hair tips to regulate root hair tip growth. Overexpression of ROP10 and a constitutively active mutant (ROP10CA) generated depolarized growth of root hairs, whereas a dominant negative mutant (ROP10DN) inhibited root hair elongation. Inoculated with Sinorhizobium meliloti, the depolarized swollen and ballooning root hairs exhibited extensive root hair deformation and aberrant infection symptoms. Upon treatment with rhizobia-secreted nodulation factors (NFs), ROP10 was transiently upregulated in root hairs, and ROP10 fused to green fluorescent protein was ectopically localized at the PM of NF-induced outgrowths and curls around rhizobia. ROP10 interacted with the kinase domain of the NF receptor NFP in a GTP-dependent manner. Moreover, NF-induced expression of the early nodulin gene ENOD11 was enhanced by the overexpression of ROP10 and ROP10CA. These data suggest that NFs spatiotemporally regulate ROP10 localization and activity at the PM of root hair tips and that interactions between ROP10 and NF receptors are required for root hair deformation and continuous curling during rhizobial infection.

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Section: Introductionmentioning

confidence: 99%

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Lei

Wang

et al. 2015

Plant Cell

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“…This interference often results in a swelling (Malhó et al, 1995;Kost et al, 1999;Parre and Geitmann, 2005a;Aouar et al, 2010;Hwang et al, 2010) or tapering ) of the tubular cell or, in extreme cases, in the arrest of growth or bursting. A phenomenon such as apical swelling is generally claimed to be the result of a depolarization of the growth process, but how intracellular events are translated into a change of cellular morphology has not been examined in detail.…”

Section: Introductionmentioning

confidence: 99%

Finite Element Model of Polar Growth in Pollen Tubes

et al. 2010

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Cellular protuberance formation in walled cells requires the local deformation of the wall and its polar expansion. In many cells, protuberance elongation proceeds by tip growth, a growth mechanism shared by pollen tubes, root hairs, and fungal hyphae. We established a biomechanical model of tip growth in walled cells using the finite element technique. We aimed to identify the requirements for spatial distribution of mechanical properties in the cell wall that would allow the generation of cellular shapes that agree with experimental observations. We based our structural model on the parameterized description of a tip-growing cell that allows the manipulation of cell size, shape, cell wall thickness, and local mechanical properties. The mechanical load was applied in the form of hydrostatic pressure. We used two validation methods to compare different simulations based on cellular shape and the displacement of surface markers. We compared the resulting optimal distribution of cell mechanical properties with the spatial distribution of biochemical cell wall components in pollen tubes and found remarkable agreement between the gradient in mechanical properties and the distribution of deesterified pectin. Use of the finite element method for the modeling of nonuniform growth events in walled cells opens future perspectives for its application to complex cellular morphogenesis in plants.

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“…Translocation and activation of ROP2 could be inhibited by coexpression with RhoGDI1 in guard cells (Jeon et al, 2008). Hwang et al (2010) demonstrated that the global inhibition of ROP1 activity by RopGAP1 and RhoGDI1 could balance the lateral propagation of apical ROP1 activation induced by overexpressing ROP1 in pollen tubes. NtRhoGDI2 has a role in recycling NtRac5 to the apex to maintain the polarity of ROP signaling and pollen tube growth .…”

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confidence: 98%

The Microtubule-Associated Protein MAP18 Affects ROP2 GTPase Activity during Root Hair Growth

et al. 2017

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Establishment and maintenance of the polar site are important for root hair tip growth. We previously reported that Arabidopsis (Arabidopsis thaliana) MICROTUBULE-ASSOCIATED PROTEIN18 (MAP18) functions in controlling the direction of pollen tube growth and root hair elongation. Additionally, the Rop GTPase ROP2 was reported as a positive regulator of both root hair initiation and tip growth in Arabidopsis. Both loss of function of ROP2 and knockdown of MAP18 lead to a decrease in root hair length, whereas overexpression of either MAP18 or ROP2 causes multiple tips or a branching hair phenotype. However, it is unclear whether MAP18 and ROP2 coordinately regulate root hair growth. In this study, we demonstrate that MAP18 and ROP2 interact genetically and functionally. MAP18 interacts physically with ROP2 in vitro and in vivo and preferentially binds to the inactive form of the ROP2 protein. MAP18 promotes ROP2 activity during root hair tip growth. Further investigation revealed that MAP18 competes with RhoGTPase GDP DISSOCIATION INHIBITOR1/SUPERCENTIPEDE1 for binding to ROP2, in turn affecting the localization of active ROP2 in the plasma membrane of the root hair tip. These results reveal a novel function of MAP18 in the regulation of ROP2 activation during root hair growth.

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Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity

Cited by 81 publications

References 45 publications

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

Finite Element Model of Polar Growth in Pollen Tubes

The Microtubule-Associated Protein MAP18 Affects ROP2 GTPase Activity during Root Hair Growth

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