Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis

The ARP2/3 complex and formins are the only known plant actin nucleators. Besides their actin-related functions, both systems also modulate microtubule organization and dynamics. Loss of the main housekeeping Arabidopsis thaliana Class I membrane-targeted formin FH1 (At3g25500) is known to increase...

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Main Authors: Petra Cifrová, Denisa Oulehlová, Eva Kollárová, Jan Martinek, Amparo Rosero, Viktor Žárský, Kateřina Schwarzerová, Fatima Cvrčková
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00148/full
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author Petra Cifrová
Denisa Oulehlová
Denisa Oulehlová
Eva Kollárová
Jan Martinek
Amparo Rosero
Viktor Žárský
Viktor Žárský
Kateřina Schwarzerová
Fatima Cvrčková
author_facet Petra Cifrová
Denisa Oulehlová
Denisa Oulehlová
Eva Kollárová
Jan Martinek
Amparo Rosero
Viktor Žárský
Viktor Žárský
Kateřina Schwarzerová
Fatima Cvrčková
author_sort Petra Cifrová
collection DOAJ
description The ARP2/3 complex and formins are the only known plant actin nucleators. Besides their actin-related functions, both systems also modulate microtubule organization and dynamics. Loss of the main housekeeping Arabidopsis thaliana Class I membrane-targeted formin FH1 (At3g25500) is known to increase cotyledon pavement cell lobing, while mutations affecting ARP2/3 subunits exhibit an opposite effect. Here we examine the role of FH1 and the ARP2/3 complex subunit ARPC5 (At4g01710) in epidermal cell morphogenesis with focus on pavement cells and trichomes using a model system of single fh1 and arpc5, as well as double fh1 arpc5 mutants. While cotyledon pavement cell shape in double mutants mostly resembled single arpc5 mutants, analysis of true leaf epidermal morphology, as well as actin and microtubule organization and dynamics, revealed a more complex relationship between the two systems and similar, rather than antagonistic, effects on some parameters. Both fh1 and arpc5 mutations increased actin network density and increased cell shape complexity in pavement cells and trichomes of first true leaves, in contrast to cotyledons. Thus, while the two actin nucleation systems have complementary roles in some aspects of cell morphogenesis in cotyledon pavement cells, they may act in parallel in other cell types and developmental stages.
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spelling doaj.art-6fcb3822acc1499486b4648a9269f2a22022-12-21T19:21:05ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-03-011110.3389/fpls.2020.00148502601Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell MorphogenesisPetra Cifrová0Denisa Oulehlová1Denisa Oulehlová2Eva Kollárová3Jan Martinek4Amparo Rosero5Viktor Žárský6Viktor Žárský7Kateřina Schwarzerová8Fatima Cvrčková9Department of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaInstitute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaInstitute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaDepartment of Experimental Plant Biology, Faculty of Science, Charles University, Prague, CzechiaThe ARP2/3 complex and formins are the only known plant actin nucleators. Besides their actin-related functions, both systems also modulate microtubule organization and dynamics. Loss of the main housekeeping Arabidopsis thaliana Class I membrane-targeted formin FH1 (At3g25500) is known to increase cotyledon pavement cell lobing, while mutations affecting ARP2/3 subunits exhibit an opposite effect. Here we examine the role of FH1 and the ARP2/3 complex subunit ARPC5 (At4g01710) in epidermal cell morphogenesis with focus on pavement cells and trichomes using a model system of single fh1 and arpc5, as well as double fh1 arpc5 mutants. While cotyledon pavement cell shape in double mutants mostly resembled single arpc5 mutants, analysis of true leaf epidermal morphology, as well as actin and microtubule organization and dynamics, revealed a more complex relationship between the two systems and similar, rather than antagonistic, effects on some parameters. Both fh1 and arpc5 mutations increased actin network density and increased cell shape complexity in pavement cells and trichomes of first true leaves, in contrast to cotyledons. Thus, while the two actin nucleation systems have complementary roles in some aspects of cell morphogenesis in cotyledon pavement cells, they may act in parallel in other cell types and developmental stages.https://www.frontiersin.org/article/10.3389/fpls.2020.00148/fullactin nucleationARP2/3At3g25500At4g01710cytoskeletonformin
spellingShingle Petra Cifrová
Denisa Oulehlová
Denisa Oulehlová
Eva Kollárová
Jan Martinek
Amparo Rosero
Viktor Žárský
Viktor Žárský
Kateřina Schwarzerová
Fatima Cvrčková
Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
Frontiers in Plant Science
actin nucleation
ARP2/3
At3g25500
At4g01710
cytoskeleton
formin
title Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
title_full Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
title_fullStr Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
title_full_unstemmed Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
title_short Division of Labor Between Two Actin Nucleators—the Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis
title_sort division of labor between two actin nucleators the formin fh1 and the arp2 3 complex in arabidopsis epidermal cell morphogenesis
topic actin nucleation
ARP2/3
At3g25500
At4g01710
cytoskeleton
formin
url https://www.frontiersin.org/article/10.3389/fpls.2020.00148/full
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