Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth

Gisbergen, Peter A.C. van; Li, Ming; Wu, Shu‐Zon; Bezanilla, Magdalena

doi:10.1083/jcb.201112085

Cited by 88 publications

(87 citation statements)

References 69 publications

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“…How these spores move without Arp2/3 is an intriguing question; perhaps they rapidly polymerize microfilaments with the aid of other nucleating machinery, such as formins (22), which are present. However, although formins in many animals, fungi, and plants are members of expanded gene families that have been differentiated to support processes required to build complex morphologies (e.g., polarized tip growth and cell plate orientation) (25,26), Porphyra has only two formins (SI Appendix, Table S15). In addition to formins, Porphyra and other red algae (SI Appendix, Tables S15 and S16) contain profilin, which interacts with formins; cofilin, a key depolymerizing factor; and severin, which cuts microfilaments to promote remodeling.…”

Section: Resultsmentioning

confidence: 99%

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Brawley¹,

Blouin²,

Ficko-Blean³

et al. 2017

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

229

222

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Porphyra umbilicalis (laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid Porphyra genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the Porphyra genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in Porphyra are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including Porphyra, lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.cytoskeleton | calcium-signaling | carbohydrate-active enzymes | stress tolerance | vitamin B 12T he red algae are one of the founding groups of photosynthetic eukaryotes (Archaeplastida) and among the few multicellular lineages within Eukarya. A red algal plastid, acquired through secondary endosymbiosis, supports carbon fixation, fatty acid synthesis, and other metabolic needs in many other algal groups in ways that are consequential. For example, diatoms and haptophytes have strong biogeochemical effects; apicomplexans cause human disease (e.g., malaria); and dinoflagellates include both coral symbionts and toxin-producing "red tides" (1). The evolutionary processes that produced the Archaeplastida and secondary algal lineages remain under investigation (2-5), but it is clear that both nuclear and plastid genes from the ancestral red algae have contributed dramatically to broader eukaryotic evolution and diversity. Consequently, the imprint of red algal metabolism on the Earth's climate system, aquatic foodwebs, and

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Section: Resultsmentioning

confidence: 99%

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Brawley¹,

Blouin²,

Ficko-Blean³

et al. 2017

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

229

222

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“…Inverted formin-2 (INF2) and formin-like protein 2 (FMNL2, also known as FRL3) are also farnesylated and myristoylated, respectively, which promotes their membrane targeting (Chhabra et al, 2009;Block et al, 2012). Moreover, mDia1 and mDia2, as well as the plant formins AFH1, formin1 and class II formin, directly bind phospholipid membranes (Cheung et al, 2010;Ramalingam et al, 2010;Gorelik et al, 2011;Martinière et al, 2011;van Gisbergen et al, 2012). These observations show that localization and activation of formins depend on their diverse interactions and that localization and activation, in some cases, serve as convergent inputs from multiple signalling pathways.…”

Section: Localization and Activation Of Forminsmentioning

confidence: 99%

Formins at a glance

Breitsprecher

Goode

2013

Journal of Cell Science

282

249

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“…To verify the expression of ROP proteins, moss protoplasts were transformed and processed for immunoblotting, as described previously (van Gisbergen et al, 2012). Immunoblotting was performed with a rabbit anti-AtROP2 serum (Zhang et al, 2010).…”

Section: Immunoblottingmentioning

confidence: 99%

A family of ROP proteins that suppress actin dynamics and are essential for polarized growth and cell adhesion

Burkart

Baskin

Bezanilla

2015

Journal of Cell Science

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In plants, the ROP family of small GTPases has been implicated in the polarized growth of tip-growing cells, such as root hairs and pollen tubes; however, most of the data derive from overexpressing ROP genes or constitutively active and dominant-negative isoforms, whereas confirmation by using loss-of-function studies has generally been lacking. Here, in the model moss Physcomitrella patens, we study ROP signaling during tip growth by using a loss-offunction approach based on RNA interference (RNAi) to silence the entire moss ROP family. We find that plants with reduced expression of ROP genes, in addition to failing to initiate tip growth, have perturbed cell wall staining, reduced cell adhesion and have increased actin-filament dynamics. Although plants subjected to RNAi against the ROP family also have reduced microtubule dynamics, this reduction is not specific to loss of ROP genes, as it occurs when actin function is compromised chemically or genetically. Our data suggest that ROP proteins polarize the actin cytoskeleton by suppressing actin-filament dynamics, leading to an increase in actin filaments at the site of polarized secretion.

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Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth

Abstract: PI(3,5)P2 is directly linked to generation and remodeling of the cortical actin array by formin during polarized cell growth in plants.

Cited by 88 publications

References 69 publications

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Formins at a glance

A family of ROP proteins that suppress actin dynamics and are essential for polarized growth and cell adhesion

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