Abstract
The actin cytoskeleton is crucial for plant morphogenesis, and organization of actin filaments (AF) is dynamically regulated by actin-binding proteins. However, the roles of actin-binding proteins, particularly type II formins, in this process remain poorly understood in plants. Here, we report that a type II formin in rice, Oryza sativa formin homolog 3 (OsFH3), acts as a major player to modulate AF dynamics and contributes to rice morphogenesis. osfh3 mutants were semi-dwarf with reduced size of seeds and unchanged responses to light or gravity compared with mutants of osfh5, another type II formin in rice. osfh3 osfh5 mutants were dwarf with more severe developmental defectiveness. Recombinant OsFH3 could nucleate actin, promote AF bundling, and cap the barbed end of AF to prevent elongation and depolymerization, but in the absence of profilin, OsFH3 could inhibit AF elongation. Different from other reported type II formins, OsFH3 could bind, but not bundle, microtubules directly. Furthermore, its N-terminal phosphatase and tensin homolog domain played a key role in modulating OsFH3 localization at intersections of AF and punctate structures of microtubules, which differed from other reported plant formins. Our results, thus, provide insights into the biological function of type II formins in modulating plant morphology by acting on AF dynamics.
Highlights
Microfilaments and microtubules are two important cytoskeletal components in plant cells
Our results demonstrate that Oryza sativa formin homolog 3 (OsFH3) contributes to rice morphology by modulating the actin filaments (AF) dynamics
The ubiquitous expression profile of OsFH3 is, consistent with those of most reported rice formins [38]; it is discrete from that of reported type II formin gene OsFH5, whose expression is observed in root tips but not in pedicle [3]
Summary
Microfilaments and microtubules are two important cytoskeletal components in plant cells. Microfilaments are actin filaments (AF) composed of polymerized globular actin (G-actin) monomers. AF elongation, bundling of filaments into cables, and cross-interaction of cables are all mediated by actin-binding proteins. Actin monomers bind to the small protein profilin, which inhibits spontaneous nucleation and elongation to sustain homeostasis, and serves as a nucleotide exchange factor for actin, increasing the exchange of ATP or ADP at least fivefold [1,2]. The AF network in plants plays indispensable roles in many biological processes, including morphogenesis [3], signal transduction [4,5], stomatal opening and closing [6], hormone signaling [7,8], immunity [9,10], organelle transport [11,12], cell division [13], and cell growth [14]. Several classes of actin-binding proteins have been implicated in AF formation, including formins, actin-related proteins-2/3 (Arp2/3), capping proteins, and enabled/vasodilator-stimulated phosphoproteins (Ena/VASP) [15,16,17,18,19]
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