Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa

Mitogen-activated protein (MAP) kinase pathways function as signaling hubs that are integral for many essential cellular processes, including sexual development. The molecular mechanisms and cross-talk between PR and CWI MAP kinase pathways have been extensively studied during asexual development. H...

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Main Authors: Nan Lan, Shuting Ye, Chengcheng Hu, Zhiling Chen, Jun Huang, Wei Xue, Shaojie Li, Xianyun Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.769615/full
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author Nan Lan
Nan Lan
Shuting Ye
Shuting Ye
Chengcheng Hu
Zhiling Chen
Jun Huang
Wei Xue
Wei Xue
Shaojie Li
Shaojie Li
Xianyun Sun
Xianyun Sun
author_facet Nan Lan
Nan Lan
Shuting Ye
Shuting Ye
Chengcheng Hu
Zhiling Chen
Jun Huang
Wei Xue
Wei Xue
Shaojie Li
Shaojie Li
Xianyun Sun
Xianyun Sun
author_sort Nan Lan
collection DOAJ
description Mitogen-activated protein (MAP) kinase pathways function as signaling hubs that are integral for many essential cellular processes, including sexual development. The molecular mechanisms and cross-talk between PR and CWI MAP kinase pathways have been extensively studied during asexual development. However, if these can be extended to sexual development remains elusive. By analyzing genome-wide transcriptional responses to deletion of each of two MAP kinase coding genes mak-2 (PR-MAP kinase pathway) and mak-1 (CWI-MAP kinase pathway) in Neurospora crassa during protoperithecium formation, 430 genes co-regulated by the MAK-1 and MAK-2 proteins were found, functionally enriched at integral components of membrane and oxidoreductase. These genes include 13 functionally known genes participating in sexual development (app, poi-2, stk-17, fsd-1, vsd-8, and NCU03863) and melanin synthesis (per-1, pkh-1, pkh-2, mld-1, scy-1, trn-2, and trn-1), as well as a set of functionally unknown genes. Phenotypic analysis of deletion mutants for the functionally unknown genes revealed that 12 genes were essential for female fertility. Among them, single-gene deletion mutants for NCU07743 (named as pfd-1), NCU02250 (oli), and NCU05948 (named as pfd-2) displayed similar protoperithecium development defects as the Δmak-1 and Δmak-2 mutants, failing to form protoperithecium. Western blotting analysis showed that both phosphorylated and total MAK-1 proteins were virtually abolished in the Δnrc-1, Δmek-2, and Δmak-2 mutants, suggesting that the posttranscriptional regulation of MAK-1 is dependent on the PR-MAP kinase pathway during the protoperithecium development. Taken together, this study revealed the regulatory roles and cross-talk between PR and CWI-MAP kinase pathways during protoperithecium development.
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spelling doaj.art-20e7a7695f044baeb7992b006aeeeee92022-12-21T23:09:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-11-011210.3389/fmicb.2021.769615769615Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassaNan Lan0Nan Lan1Shuting Ye2Shuting Ye3Chengcheng Hu4Zhiling Chen5Jun Huang6Wei Xue7Wei Xue8Shaojie Li9Shaojie Li10Xianyun Sun11Xianyun Sun12Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, Capital Normal University, Beijing, ChinaShandong Jinniu Group Company, Ltd., Jinan, ChinaInstitute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing, ChinaMitogen-activated protein (MAP) kinase pathways function as signaling hubs that are integral for many essential cellular processes, including sexual development. The molecular mechanisms and cross-talk between PR and CWI MAP kinase pathways have been extensively studied during asexual development. However, if these can be extended to sexual development remains elusive. By analyzing genome-wide transcriptional responses to deletion of each of two MAP kinase coding genes mak-2 (PR-MAP kinase pathway) and mak-1 (CWI-MAP kinase pathway) in Neurospora crassa during protoperithecium formation, 430 genes co-regulated by the MAK-1 and MAK-2 proteins were found, functionally enriched at integral components of membrane and oxidoreductase. These genes include 13 functionally known genes participating in sexual development (app, poi-2, stk-17, fsd-1, vsd-8, and NCU03863) and melanin synthesis (per-1, pkh-1, pkh-2, mld-1, scy-1, trn-2, and trn-1), as well as a set of functionally unknown genes. Phenotypic analysis of deletion mutants for the functionally unknown genes revealed that 12 genes were essential for female fertility. Among them, single-gene deletion mutants for NCU07743 (named as pfd-1), NCU02250 (oli), and NCU05948 (named as pfd-2) displayed similar protoperithecium development defects as the Δmak-1 and Δmak-2 mutants, failing to form protoperithecium. Western blotting analysis showed that both phosphorylated and total MAK-1 proteins were virtually abolished in the Δnrc-1, Δmek-2, and Δmak-2 mutants, suggesting that the posttranscriptional regulation of MAK-1 is dependent on the PR-MAP kinase pathway during the protoperithecium development. Taken together, this study revealed the regulatory roles and cross-talk between PR and CWI-MAP kinase pathways during protoperithecium development.https://www.frontiersin.org/articles/10.3389/fmicb.2021.769615/fullMAP kinasesexual developmentprotoperitheciumMAK-1MAK-2Neurospora crassa
spellingShingle Nan Lan
Nan Lan
Shuting Ye
Shuting Ye
Chengcheng Hu
Zhiling Chen
Jun Huang
Wei Xue
Wei Xue
Shaojie Li
Shaojie Li
Xianyun Sun
Xianyun Sun
Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
Frontiers in Microbiology
MAP kinase
sexual development
protoperithecium
MAK-1
MAK-2
Neurospora crassa
title Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
title_full Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
title_fullStr Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
title_full_unstemmed Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
title_short Coordinated Regulation of Protoperithecium Development by MAP Kinases MAK-1 and MAK-2 in Neurospora crassa
title_sort coordinated regulation of protoperithecium development by map kinases mak 1 and mak 2 in neurospora crassa
topic MAP kinase
sexual development
protoperithecium
MAK-1
MAK-2
Neurospora crassa
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.769615/full
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