Control of Pollen Tube Tip Growth by a Rop GTPase–Dependent Pathway That Leads to Tip-Localized Calcium Influx

Li, Hai; Lin, Yong; Heath, Rachel M.; Zhu, Michael X.; Yang, Zhenbiao

doi:10.1105/tpc.11.9.1731

Cited by 349 publications

(511 citation statements)

References 46 publications

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“…Kawasaki et al (1999) provided evidence that OsRAC1 could be a regulator of an NADPH oxidase, as known for RAC2 and RAC1 from mammalian systems (Bokoch and Diebold, 2002). Like RAC/ROP proteins (Li et al, 1999), the NADPH oxidase is involved in ROI production and tip-focused Ca 2 accumulation during polar root hair growth (Foreman et al, 2003). The establishment of Bgh-haustoria in barley epidermal cells requires polar plant membrane growth, and during this process, generation of superoxide at the side of penetration has been detected.…”

Section: Discussionmentioning

confidence: 99%

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

et al. 2003

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SummarySmall monomeric G-proteins of the plant ras (rat sarcome oncogene product) related C3 botulinum toxin substrate (RAC)/Rho of plants (ROP) family are molecular switches in signal transduction of many cellular processes. RAC/ROPs regulate hormone effects, subcellular gradients of Ca 2 , the organisation of the actin cytoskeleton and the production of reactive oxygen intermediates. Therefore, we followed a genetic bottom-up strategy to study the role of these proteins during the interaction of barley (Hordeum vulgare L.) with the fungal biotrophic pathogen Blumeria graminis f.sp. hordei (Bgh). We identi®ed six barley RAC/ ROP proteins and studied their gene expression. Five out of six Rac/Rop genes were expressed constitutively in the leaf epidermis, which is the site of interaction with Bgh. None of the genes showed enhancement of mRNA abundance after inoculation with Bgh. After microprojectile mediated transformation of single barley epidermal cells with constitutively activated mutant RAC/ROP proteins, we found an RAC/ ROP-speci®c enhancement of pathogen accessibility, tagging HvRACB, HvRAC3 and HvROP6 as host proteins potentially involved in the establishment of susceptibility to Bgh. Confocal laser scanning microscopy (CLSM) of green¯uorescent protein (GFP):HvRAC/ROP-transformed cells revealed varying strengths of plasma membrane association of barley RAC/ROPs. The C-terminal CAAX motif for presumable prenylation or the C-terminal hypervariable region (HVR), respectively, were required for membrane association of the RAC/ROPs. Proper intracellular localisation was essential for HvRACB and HvRAC3 function. Together, our data support the view that different paths of host signal transduction via RAC/ROP G-proteins are involved in processes supporting parasitic entry into epidermal host cells.

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Section: Discussionmentioning

confidence: 99%

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

et al. 2003

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“…ROPs and Rabs have been shown to localize to the tips of root hairs and pollen tubes (Molendijk et al, 2001;Jones et al, 2002;Preuss et al, 2004), and consistent with its proposed function in polarized growth, tip localization of Rab4Ab was only observed in growing root hairs but not in mature root hairs that had ceased growing or root hair mutants with defective tip growth (Preuss et al, 2004). Furthermore, constitutively active or dominant negative ROPs altered tip growth, resulting in the formation of bulbous tips in pollen tubes (Kost et al, 1999;Li et al, 1999) and root hairs with wavy growth, multiple tips, and partially swollen tips (Molendijk et al, 2001;Jones et al, 2002;Bloch et al, 2005). Disrupting ROP GTPase function by the expression of constitutively active or dominant negative ROP has been shown to affect apical F-actin dynamics, calcium signaling, and ROS production.…”

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confidence: 94%

A Class I ADP-Ribosylation Factor GTPase-Activating Protein Is Critical for Maintaining Directional Root Hair Growth in Arabidopsis

et al. 2008

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Membrane trafficking and cytoskeletal dynamics are important cellular processes that drive tip growth in root hairs. These processes interact with a multitude of signaling pathways that allow for the efficient transfer of information to specify the direction in which tip growth occurs. Here, we show that AGD1, a class I ADP ribosylation factor GTPase-activating protein, is important for maintaining straight growth in Arabidopsis (Arabidopsis thaliana) root hairs, since mutations in the AGD1 gene resulted in wavy root hair growth. Live cell imaging of growing agd1 root hairs revealed bundles of endoplasmic microtubules and actin filaments extending into the extreme tip. The wavy phenotype and pattern of cytoskeletal distribution in root hairs of agd1 partially resembled that of mutants in an armadillo repeat-containing kinesin (ARK1). Root hairs of double agd1 ark1 mutants were more severely deformed compared with single mutants. Organelle trafficking as revealed by a fluorescent Golgi marker was slightly inhibited, and Golgi stacks frequently protruded into the extreme root hair apex of agd1 mutants. Transient expression of green fluorescent protein-AGD1 in tobacco (Nicotiana tabacum) epidermal cells labeled punctate bodies that partially colocalized with the endocytic marker FM4-64, while ARK1-yellow fluorescent protein associated with microtubules. Brefeldin A rescued the phenotype of agd1, indicating that the altered activity of an AGD1-dependent ADP ribosylation factor contributes to the defective growth, organelle trafficking, and cytoskeletal organization of agd1 root hairs. We propose that AGD1, a regulator of membrane trafficking, and ARK1, a microtubule motor, are components of converging signaling pathways that affect cytoskeletal organization to specify growth orientation in Arabidopsis root hairs.

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“…In vitro pollen germination and pollen tube growth were analyzed as described previously (Li et al, 1999) with some modifications. Flowers collected from Arabidopsis plants 1 to 2 weeks after bolting were used for the examinations.…”

Section: In Vitro Pollen Germination and Growth Measurementmentioning

confidence: 99%

The Arabidopsis Phosphatidylinositol 3-Kinase Is Important for Pollen Development

et al. 2008

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Phosphatidylinositol 3-kinase has been reported to be important for normal plant growth. To characterize the role of the enzyme further, we attempted to isolate Arabidopsis (Arabidopsis thaliana) plants that do not express the gene, but we could not recover homozygous mutant plants. The progeny of VPS34/vps34 heterozygous plants, harboring a T-DNA insertion, showed a segregation ratio of 1:1:0 for wild-type, heterozygous, and homozygous mutant plants, indicating a gametophytic defect. Genetic transmission analysis showed that the abnormal segregation ratio was due to failure to transmit the mutant allele through the male gametophyte. Microscopic observation revealed that 2-fold higher proportions of pollen grains in heterozygous plants than wild-type plants were dead or showed reduced numbers of nuclei. Many mature pollen grains from the heterozygous plants contained large vacuoles even until the mature pollen stage, whereas pollen from wild-type plants contained many small vacuoles beginning from the vacuolated pollen stage, which indicated that vacuoles in many of the heterozygous mutant pollen did not undergo normal fission after the first mitotic division. Taken together, our results suggest that phosphatidylinositol 3-kinase is essential for vacuole reorganization and nuclear division during pollen development.

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Control of Pollen Tube Tip Growth by a Rop GTPase–Dependent Pathway That Leads to Tip-Localized Calcium Influx

Cited by 349 publications

References 46 publications

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

A Class I ADP-Ribosylation Factor GTPase-Activating Protein Is Critical for Maintaining Directional Root Hair Growth in Arabidopsis

The Arabidopsis Phosphatidylinositol 3-Kinase Is Important for Pollen Development

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