Higher-Ordered Actin Structures Remodeled by Arabidopsis ACTIN-DEPOLYMERIZING FACTOR5 Are Important for Pollen Germination and Pollen Tube Growth

Abstract

Dynamics of the actin cytoskeleton are essential for pollen germination and pollen tube growth. ACTIN-DEPOLYMERIZING FACTORs (ADFs) typically contribute to actin turnover by severing/depolymerizing actin filaments. Recently, we demonstrated that Arabidopsis subclass III ADFs (ADF5 and ADF9) evolved F-actin-bundling function from conserved F-actin-depolymerizing function. However, little is known about the physiological function, the evolutional significance, and the actin-bundling mechanism of these neofunctionalized ADFs. Here, we report that loss of ADF5 function caused delayed pollen germination, retarded pollen tube growth, and increased sensitive to latrunculin B (LatB) treatment by affecting the generation and maintenance of actin bundles. Examination of actin filament dynamics in living cells revealed that the bundling frequency was significantly decreased in adf5 pollen tubes, consistent with its biochemical functions. Further biochemical and genetic complementation analyses demonstrated that both the N- and C-terminal actin-binding domains of ADF5 are required for its physiological and biochemical functions. Interestingly, while both are atypical actin-bundling ADFs, ADF5, but not ADF9, plays an important role in mature pollen physiological activities. Taken together, our results suggest that ADF5 has evolved the function of bundling actin filaments and plays an important role in the formation, organization, and maintenance of actin bundles during pollen germination and pollen tube growth.

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

“…The actin cytoskeleton is a highly dynamic structure that enables rapid responses to intracellular signaling molecules and regulatory proteins (Staiger et al, 1997;Zhu et al, 2013). It has been demonstrated that dynamic actin cytoskeleton rearrangements are regulated by a pool of actin-binding proteins and phytohormones (Hussey et al, 2006;Lanza et al, 2012;Jia et al, 2013;Zhu et al, 2017). Additionally, proteomic studies have shown that cytoskeletal proteins are regulated by a variety of posttranslational modifications, including phosphorylation, S-glutathionylation, nitration, S-sulfhydration, and S-nitrosylation (Lam et al, 2010;Yemets et al, 2011).…”

Genome-Wide Identification and Characterization of Actin-Depolymerizing Factor (ADF) Family Genes and Expression Analysis of Responses to Various Stresses in Zea Mays L.

“…During pollen germination and pollen tube growth, AtADF5, but not AtADF9, makes an important impact in the formation, organization, and maintenance of actin bundles [30]. The loss-function mutant of pollen specifically expresses AtADF7 which significantly suppresses the pollen tube growth [31] and AtADF10 is a pollen-specific ADF, however, AtADF7 and AtADF10 show different spatial profiles, indicating their unique functions in the pollen tube for regulating actin dynamics [16].…”

Actin Polymerization Mediated by AtFH5 Directs the Polarity Establishment and Vesicle Trafficking for Pollen Germination in Arabidopsis

“…The dynamics of the actin cytoskeleton are precisely regulated by a group of actin binding proteins (ABPs) (Ren and Xiang., 2007;Li et al, 2015). Several studies have found that the mutation of some ABPs, such as FIMBRIN5 (FIM5) and ACTIN-DEPOLYMERIZING FACTOR5 (ADF5), causes abnormal actin filaments in pollen grains and impairs germination Zhu et al, 2017). Formin is a potent actin nucleator that stabilizes the formation of actin nuclei and induces the assembly of parallel actin filaments for the formation of actin bundles or cables (A) Representative time-lapse images (maximal projection of z sections of the whole cell) of actin filaments labeled with Lifeact-mEGFP during pollen germination.…”