The canonical α-SNAP is essential for gametophytic development in Arabidopsis

Liu, Fei; Li, Jipeng; Li, Lushen; Liu, Qi; Li, Shan-Wei; Song, Minglei; Li, Sha; Zhang, Yan

doi:10.1371/journal.pgen.1009505

Cited by 12 publications

(13 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Roles for these proteins in the Arabidopsis fusion apparatus have not been reported, but a role in gametogenesis for ASNAP/ALPHA-SNAP2 has been established by Liu et al . [35]. Finally, both ASNAP1 and ASNAP2 transcripts are present in Arabidopsis guard cells [36,37].…”

Section: Resultsmentioning

confidence: 99%

Model-based inference of a plant-specific dual role for HOPS in regulating guard cell vacuole fusion

Hodgens,

Flaherty,

Pullen

et al. 2023

Preprint

View full text Add to dashboard Cite

Stomata are the pores on a leaf surface that regulate gas exchange. Each stoma consists of two guard cells whose movements regulate pore opening and thereby control CO2fixation and water loss. Guard cell movements depend in part on the remodeling of vacuoles, which have been observed to change from a highly fragmented state to a fused morphology during stomata opening. This change in morphology requires a membrane fusion mechanism that responds rapidly to environmental signals, allowing plants to respond to diurnal and stress cues. With guard cell vacuoles being both large and responsive to external signals, stomata represent a unique system in which to delineate mechanisms of membrane fusion.Fusion of vacuole membranes is a highly conserved process in eukaryotes, with key roles played by two multi-subunit complexes: HOPS (homotypic fusion and vacuolar protein sorting) and SNARE (soluble NSF attachment protein receptor). HOPS is a vacuole tethering factor that is thought to chaperone SNAREs from apposing vacuole membranes into a fusion-competent complex capable of rearranging membranes. To resolve a counter-intuitive observation regarding the role of HOPS in regulating plant vacuole morphology, we derived a quantitative model of vacuole fusion dynamics and used it to generate testable predictions about HOPS-SNARE interactions. We derived our model by applying simulation-based inference to integrate prior knowledge about molecular interactions with limited, qualitative observations of emergent vacuole phenotypes. By constraining the model parameters to yield the emergent outcomes observed for stoma opening – as induced by two distinct chemical treatments – we predicted a dual role for HOPS and identified a stalled form of the SNARE complex that differs from phenomena reported in yeast. We predict that HOPS has contradictory actions at different points in the fusion signaling pathway, promoting the formation of SNARE complexes, but limiting their activity.Author summaryPlants “breathe” through pores in their leaves where each pore is formed by two specialized cells called guard cells. To open these pores, guard cells change in volume. This volume change is controlled by water-filled organelles called vacuoles that morph from multiple small entities to a few large ones capable of taking up more water to reshape the cell. Specialized proteins in vacuole membranes make this change happen by pulling vacuoles together until they fuse. Some of these proteins reside in membranes, but others must be drawn to the membrane from the cell’s cytoplasm. Specific lipid molecules in the membrane play an important role in recruiting those proteins to the vacuole membrane. We previously made an unexpected finding that removing this lipid induces plant vacuole fusion. To make sense of this observation, we used a mathematical model to piece together our knowledge of the proteins involved in this process and what we know about the chemical treatments that cause vacuoles to morph. Using computer simulations, we uncovered new rules about how molecules interact in membranes to accomplish the task of vacuole fusion in plants. We think the rules uncovered through mathematical modeling allow plants to respond quickly to environmental cues.

show abstract

Section: Resultsmentioning

confidence: 99%

Model-based inference of a plant-specific dual role for HOPS in regulating guard cell vacuole fusion

Hodgens,

Flaherty,

Pullen

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The only NSF mutants described in Arabidopsis display mild leaf serration defects (Tang et al, 2020) or cause abnormal Golgi morphology (Tanabashi et al, 2018). By contrast, CRISPR/Cas9-generated αSNAP pre-mature stop codon mutants appear to be gametophytically lethal (Liu et al, 2021). There are no T-DNA insertion knockout alleles of NSF and CRISPR/Cas9 deletions of NSF appeared not to be transmissible (M.P and G.J, unpublished observation), suggesting that knockouts of αSNAP2-interacting NSF might also be gametophytically lethal (Liu et al, 2021).…”

Section: Resultsmentioning

confidence: 99%

“…By contrast, CRISPR/Cas9-generated αSNAP pre-mature stop codon mutants appear to be gametophytically lethal (Liu et al, 2021). There are no T-DNA insertion knockout alleles of NSF and CRISPR/Cas9 deletions of NSF appeared not to be transmissible (M.P and G.J, unpublished observation), suggesting that knockouts of αSNAP2-interacting NSF might also be gametophytically lethal (Liu et al, 2021). We therefore generated transgenic plants that overexpressed engineered dominant-negative variants conditionally.…”

Section: Resultsmentioning

confidence: 99%

NSF/αSNAP2-mediated cis-SNARE complex disassembly precedes membrane fusion generating the cell plate during Arabidopsis cytokinesis

Park

Mayer

Jürgens

2022

Preprint

View full text Add to dashboard Cite

SummaryEukaryotic membrane fusion requires trans-SNARE complexes bridging the gap between adjacent membranes (Jahn and Scheller, 2006). Fusion between a transport vesicle and its target membrane transforms the trans-into a cis-SNARE complex. The latter interacts with the hexameric AAA+-ATPase NSF and its co-factor αSNAP, forming a 20S complex (Zhou et al., 2015; Zhao and Brunner, 2016). ATPase activity disassembles the SNARE complex into Qa-SNARE, which folds back onto itself, and its partners (Huang et al., 2019; Kim et al., 2021). Fusion of identical membranes has a different sequence of events (Baker and Hughson, 2016). The fusion partners each have cis-SNARE complexes to be broken up by NSF and αSNAP. The Qa-SNARE monomers are then stabilized by interaction with Sec1-type regulators (SM proteins) to form trans-SNARE complexes, as shown for the yeast vacuole (Baker et al., 2015). Membrane fusion in Arabidopsis cytokinesis is formally akin to vacuolar fusion (Müller and Jürgens, 2016). Membrane vesicles fuse with one another to form the partitioning membrane known as cell plate. Cis-SNARE complexes of cytokinesis-specific Qa-SNARE KNOLLE and its SNARE partners are assembled at the ER and delivered by traffic via Golgi/TGN to the cell division plane (Karnahl and Park et al., 2017). SM protein KEULE is required for the formation of trans-SNARE complexes between adjacent membrane vesicles (Park et al., 2012). Here, we identify the missing NSF-type AAA+-ATPase and its adaptor αSNAP2 required for disassembly of KNOLLE cis-SNARE complexes. In addition, we show that NSF is also required for other trafficking pathways and interacts with the respective Q-SNAREs. In conclusion, the SNARE complex disassembly machinery is conserved in plants and plays a unique essential role in cytokinesis.

show abstract

“…Pollen development, including DAPI staining, Alexander staining, scanning electron microscope (SEM) of developing anthers, optical sectioning, and transverse sectioning, was as described [30][31][32][33][34]. Methods to analyse pollen germination in vitro and aniline blue staining at 48 HAP were performed as described [30][31][32][33][34]. For each pistil, about 20-30 pollen grains from designated genotypes were put on stigma under a stereoscope.…”

Section: Phenotype Analysismentioning

confidence: 99%

ArabidopsisRAN GTPases are critical for mitosis during male and female gametogenesis

Qin

Sun

et al. 2022

FEBS Letters

Self Cite

View full text Add to dashboard Cite

The development of male and female gametophytes is a prerequisite for successful propagation of angiosperms. The small GTPases RAN play fundamental roles in numerous cellular processes. Although RAN GTPases have been characterized in plants, their roles in cellular processes are far from understood. We report here that RAN GTPases in Arabidopsis are critical for gametophytic development. RAN1 loss‐of‐function showed no defects in gametophytic development likely due to redundancy. However, the expression of a dominant negative or constitutively active RAN1 resulted in gametophytic lethality. Genetic interference of RAN GTPases caused the arrest of pollen mitosis I and of mitosis of functional megaspores, implying a key role of properly regulated RAN activity in mitosis during gametophytic development.

show abstract

The canonical α-SNAP is essential for gametophytic development in Arabidopsis

Cited by 12 publications

References 67 publications

Model-based inference of a plant-specific dual role for HOPS in regulating guard cell vacuole fusion

Model-based inference of a plant-specific dual role for HOPS in regulating guard cell vacuole fusion

NSF/αSNAP2-mediated cis-SNARE complex disassembly precedes membrane fusion generating the cell plate during Arabidopsis cytokinesis

ArabidopsisRAN GTPases are critical for mitosis during male and female gametogenesis

Contact Info

Product

Resources

About