HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa

Jonkers, Wilfried; Leeder, Abigail C.; Ansong, Charles; Wang, Yuexi; Yang, Feng; Starr, Trevor L.; Camp, II, David G.; Smith, Richard D.; Glass, N. Louise; Heitman, Joseph

doi:10.1371/journal.pgen.1004783

Title: HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa

Journal Article · Thu Nov 20 00:00:00 EST 2014 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1004783· OSTI ID:1166844

Jonkers, Wilfried ^[1]; Leeder, Abigail C. ^[1]; Ansong, Charles ^[2]; Wang, Yuexi ^[2]; Yang, Feng ^[3]; Starr, Trevor L. ^[1]; Camp, II, David G. ^[2]; Smith, Richard D. ^[2]; Glass, N. Louise ^[1]; Heitman, Joseph ^[4]

Univ. of California, Berkeley, CA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Genentech, South San Francisco, CA (United States)
Duke Univ. Medical Center, Durham, NC (United States)

© 2014. Cell fusion in genetically identical Neurospora crassa germlings and in hyphae is a highly regulated process involving the activation of a conserved MAP kinase cascade that includes NRC-1, MEK-2 and MAK-2. During chemotrophic growth in germlings, the MAP kinase cascade members localize to conidial anastomosis tube (CAT) tips every ~8 minutes, perfectly out of phase with another protein that is recruited to the tip: SOFT, a recently identified scaffold for the MAK-1 MAP kinase pathway in Sordaria macrospora. How the MAK-2 oscillation process is initiated, maintained and what proteins regulate the MAP kinase cascade is currently unclear. A global phosphoproteomics approach using an allele of mak-2 (mak-2 Q100G ) that can be specifically inhibited by the ATP analog 1NM-PP1 was utilized to identify MAK-2 kinase targets in germlings that were potentially involved in this process. One such putative target was HAM-5, a protein of unknown biochemical function. Previously, Δham-5 mutants were shown to be deficient for hyphal fusion. Here we show that HAM-5-GFP co-localized with NRC-1, MEK-2 and MAK-2 and oscillated with identical dynamics from the cytoplasm to CAT tips during chemotropic interactions. In the Δmak-2 strain, HAM-5-GFP localized to punctate complexes that did not oscillate, but still localized to the germling tip, suggesting that MAK-2 activity influences HAM-5 function/localization. However, MAK-2-GFP showed cytoplasmic and nuclear localization in a Δham-5 strain and did not localize to puncta. Via co-immunoprecipitation experiments, HAM-5 was shown to physically interact with NRC-1, MEK-2 and MAK-2, suggesting that it functions as a scaffold/transport hub for the MAP kinase cascade members for oscillation and chemotropic interactions during germling and hyphal fusion in N. crassa. The identification of HAM-5 as a scaffold-like protein will help to link the activation of MAK-2 cascade to upstream factors and proteins involved in this intriguing process of fungal communication.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231

OSTI ID:: 1166844

Alternate ID(s):: OSTI ID: 1407220

Report Number(s):: PNNL-SA-103955; 48135; 400412000

Journal Information:: PLoS Genetics, Vol. 10, Issue 11; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 55 works

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Regulation of Cell-to-Cell Communication and Cell Wall Integrity by a Network of MAP Kinase Pathways and Transcription Factors in Neurospora crassa Fischer, Monika S.; Wu, Vincent W.; Lee, Ji E. Genetics, Vol. 209, Issue 2 https://doi.org/10.1534/genetics.118.300904	journal	April 2018
Integration of Self and Non-self Recognition Modulates Asexual Cell-to-Cell Communication in Neurospora crassa Fischer, Monika S.; Jonkers, Wilfried; Glass, N. Louise Genetics, Vol. 211, Issue 4 https://doi.org/10.1534/genetics.118.301780	journal	February 2019
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The Neurospora Transcription Factor ADV-1 Transduces Light Signals and Temporal Information to Control Rhythmic Expression of Genes Involved in Cell Fusion Dekhang, Rigzin; Wu, Cheng; Smith, Kristina M. G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 1 https://doi.org/10.1534/g3.116.034298	journal	November 2016
Communicate and Fuse: How Filamentous Fungi Establish and Maintain an Interconnected Mycelial Network Fischer, Monika S.; Glass, N. Louise Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00619	journal	March 2019
WHI-2 Regulates Intercellular Communication via a MAP Kinase Signaling Complex Gonçalves, A. Pedro; Chow, Karen M.; Cea-Sánchez, Sara Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.03162	journal	January 2020

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60 APPLIED LIFE SCIENCES
Environmental Molecular Sciences Laboratory
cell fusion
phosphorylation
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genetic oscillators
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