Microtubules are required for motility and positioning of vesicles and mitochondria in hyphal tip cells of Allomyces macrogynus

Dennis P. McDaniel, Robert Roberson

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

We have used video-enhanced light microscopy and digital image processing to characterize the intracellular motility and positioning of vesicles (∼1-μm diameter) and mitochondria in growing hyphal tip cells of Allomyces macrogynus. These observations were coupled with cytoskeletal inhibitory experiments to define the roles of the microtubule and actin cytoskeletons in organelle translocation and positioning. Vesicles and mitochondria were abundant in apical and subapical hypha regions. Vesicles traveled along paths that were parallel to the longitudinal axis of the cell. Anterograde (i.e., toward the hyphal apex) and retrograde (i.e., away from the hyphal apex) movements of vesicles occurred at average rates of 4.0 and 2.2 μm/s, respectively. Bidirectional travel of vesicles along common paths was noted in the cortical cytoplasm. Mitochondria were aligned mostly parallel to the long axis of the hypha, except those extending into the hyphal apex, which were oriented toward the Spitzenkörper. In regions of the subapical hypha mitochondria were often restricted to the cortical cytoplasm and nuclei occupied the central cytoplasmic region. Mitochondria displayed rapid anterograde movements reaching speeds of 3.0 μm/s, but primarily maintained a constant position relative to either the advancing cytoplasm or the lateral cell wall. Cytoskeletal disruption experiments showed that the positioning of mitochondria and motility of vesicles and mitochondria were microtubule-based and suggested that the actin cytoskeleton played uncertain roles.

Original languageEnglish (US)
Pages (from-to)233-244
Number of pages12
JournalFungal Genetics and Biology
Volume31
Issue number3
DOIs
StatePublished - 2000

Fingerprint

Allomyces
Microtubules
Mitochondria
Hyphae
Cytoplasm
Actin Cytoskeleton
Organelles
Cell Wall
Microscopy
Light

Keywords

  • Cytoskeleton
  • Hyphal tip growth
  • Intracellular motility
  • Video-enhanced light microscopy

ASJC Scopus subject areas

  • Genetics
  • Microbiology

Cite this

@article{e35d20d34f5343cb8e3651f1302d0827,
title = "Microtubules are required for motility and positioning of vesicles and mitochondria in hyphal tip cells of Allomyces macrogynus",
abstract = "We have used video-enhanced light microscopy and digital image processing to characterize the intracellular motility and positioning of vesicles (∼1-μm diameter) and mitochondria in growing hyphal tip cells of Allomyces macrogynus. These observations were coupled with cytoskeletal inhibitory experiments to define the roles of the microtubule and actin cytoskeletons in organelle translocation and positioning. Vesicles and mitochondria were abundant in apical and subapical hypha regions. Vesicles traveled along paths that were parallel to the longitudinal axis of the cell. Anterograde (i.e., toward the hyphal apex) and retrograde (i.e., away from the hyphal apex) movements of vesicles occurred at average rates of 4.0 and 2.2 μm/s, respectively. Bidirectional travel of vesicles along common paths was noted in the cortical cytoplasm. Mitochondria were aligned mostly parallel to the long axis of the hypha, except those extending into the hyphal apex, which were oriented toward the Spitzenk{\"o}rper. In regions of the subapical hypha mitochondria were often restricted to the cortical cytoplasm and nuclei occupied the central cytoplasmic region. Mitochondria displayed rapid anterograde movements reaching speeds of 3.0 μm/s, but primarily maintained a constant position relative to either the advancing cytoplasm or the lateral cell wall. Cytoskeletal disruption experiments showed that the positioning of mitochondria and motility of vesicles and mitochondria were microtubule-based and suggested that the actin cytoskeleton played uncertain roles.",
keywords = "Cytoskeleton, Hyphal tip growth, Intracellular motility, Video-enhanced light microscopy",
author = "McDaniel, {Dennis P.} and Robert Roberson",
year = "2000",
doi = "10.1006/fgbi.2000.1249",
language = "English (US)",
volume = "31",
pages = "233--244",
journal = "Fungal Genetics and Biology",
issn = "1087-1845",
publisher = "Academic Press Inc.",
number = "3",

}

TY - JOUR

T1 - Microtubules are required for motility and positioning of vesicles and mitochondria in hyphal tip cells of Allomyces macrogynus

AU - McDaniel, Dennis P.

AU - Roberson, Robert

PY - 2000

Y1 - 2000

N2 - We have used video-enhanced light microscopy and digital image processing to characterize the intracellular motility and positioning of vesicles (∼1-μm diameter) and mitochondria in growing hyphal tip cells of Allomyces macrogynus. These observations were coupled with cytoskeletal inhibitory experiments to define the roles of the microtubule and actin cytoskeletons in organelle translocation and positioning. Vesicles and mitochondria were abundant in apical and subapical hypha regions. Vesicles traveled along paths that were parallel to the longitudinal axis of the cell. Anterograde (i.e., toward the hyphal apex) and retrograde (i.e., away from the hyphal apex) movements of vesicles occurred at average rates of 4.0 and 2.2 μm/s, respectively. Bidirectional travel of vesicles along common paths was noted in the cortical cytoplasm. Mitochondria were aligned mostly parallel to the long axis of the hypha, except those extending into the hyphal apex, which were oriented toward the Spitzenkörper. In regions of the subapical hypha mitochondria were often restricted to the cortical cytoplasm and nuclei occupied the central cytoplasmic region. Mitochondria displayed rapid anterograde movements reaching speeds of 3.0 μm/s, but primarily maintained a constant position relative to either the advancing cytoplasm or the lateral cell wall. Cytoskeletal disruption experiments showed that the positioning of mitochondria and motility of vesicles and mitochondria were microtubule-based and suggested that the actin cytoskeleton played uncertain roles.

AB - We have used video-enhanced light microscopy and digital image processing to characterize the intracellular motility and positioning of vesicles (∼1-μm diameter) and mitochondria in growing hyphal tip cells of Allomyces macrogynus. These observations were coupled with cytoskeletal inhibitory experiments to define the roles of the microtubule and actin cytoskeletons in organelle translocation and positioning. Vesicles and mitochondria were abundant in apical and subapical hypha regions. Vesicles traveled along paths that were parallel to the longitudinal axis of the cell. Anterograde (i.e., toward the hyphal apex) and retrograde (i.e., away from the hyphal apex) movements of vesicles occurred at average rates of 4.0 and 2.2 μm/s, respectively. Bidirectional travel of vesicles along common paths was noted in the cortical cytoplasm. Mitochondria were aligned mostly parallel to the long axis of the hypha, except those extending into the hyphal apex, which were oriented toward the Spitzenkörper. In regions of the subapical hypha mitochondria were often restricted to the cortical cytoplasm and nuclei occupied the central cytoplasmic region. Mitochondria displayed rapid anterograde movements reaching speeds of 3.0 μm/s, but primarily maintained a constant position relative to either the advancing cytoplasm or the lateral cell wall. Cytoskeletal disruption experiments showed that the positioning of mitochondria and motility of vesicles and mitochondria were microtubule-based and suggested that the actin cytoskeleton played uncertain roles.

KW - Cytoskeleton

KW - Hyphal tip growth

KW - Intracellular motility

KW - Video-enhanced light microscopy

UR - http://www.scopus.com/inward/record.url?scp=0034466109&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0034466109&partnerID=8YFLogxK

U2 - 10.1006/fgbi.2000.1249

DO - 10.1006/fgbi.2000.1249

M3 - Article

C2 - 11273684

AN - SCOPUS:0034466109

VL - 31

SP - 233

EP - 244

JO - Fungal Genetics and Biology

JF - Fungal Genetics and Biology

SN - 1087-1845

IS - 3

ER -