Arabidopsis QWRF1 and QWRF2 Redundantly Modulate Cortical Microtubule Arrangement in Floral Organ Growth and Fertility

Abstract

Floral organ development is fundamental to sexual reproduction in angiosperms. Many key floral regulators (most of which are transcription factors) have been identified and shown to modulate floral meristem determinacy and floral organ identity, but not much is known about the regulation of floral organ growth, which is a critical process by which organs to achieve appropriate morphologies and fulfill their functions. Spatial and temporal control of anisotropic cell expansion following initial cell proliferation is important for organ growth. Cortical microtubules are well known to have important roles in plant cell polar growth/expansion and have been reported to guide the growth and shape of sepals and petals. In this study, we identified two homolog proteins, QWRF1 and QWRF2, which are essential for floral organ growth and plant fertility. We found severely deformed morphologies and symmetries of various floral organs as well as a significant reduction in the seed setting rate in the qwrf1qwrf2 double mutant, although few flower development defects were seen in qwrf1 or qwrf2 single mutants. QWRF1 and QWRF2 display similar expression patterns and are both localized to microtubules in vitro and in vivo. Furthermore, we found altered cortical microtubule organization and arrangements in qwrf1qwrf2 cells, consistent with abnormal cell expansion in different floral organs, which eventually led to poor fertility. Our results suggest that QWRF1 and QWRF2 are likely microtubule-associated proteins with functional redundancy in fertility and floral organ development, which probably exert their effects via regulation of cortical microtubules and anisotropic cell expansion.

Microtubule Regulation in Plants: From Morphological Development to Stress Adaptation

“…Cortical MTs play important roles in plant cell polar growth/expansion and have been reported to guide the growth and shape of sepals and petals [ 139 ]. MAPs were found to modulate cortical MT arrangement in flower organ growth and fertility: Increased Petal Growth Anisotropy 1, QWRF1, and QWRF2 affect MT organization and stability to regulate petal growth anisotropy [ 140 , 141 ], and KATANIN 1 mediates MT organization to regulate petal conical cell shape [ 142 , 143 ] and the pollen tube path [ 144 ]. KATANIN 1-mediated MT severing is critical for stamen filament development, as shown by the crosstalk between MT severing and BR signaling [ 145 ].…”

The role of intrinsic disorder in binding of plant microtubule‐associated proteins to the cytoskeleton

“…With some exceptions, MTs consist of 13 protofilaments that are parallelly aligned, forming hollow scaffolding cylinders of about 24 nm in diameter (Goodson & Jonasson, 2018; Hashimoto, 2015). The MT cytoskeleton is essential for various critical cell functions, as cell division, vesicle, and organelle transport (Goodson & Jonasson, 2018; Motta & Schnittger, 2021) and readily responds to environmental stress and endogenous factors that influence their function and dynamics (Chen et al, 2016; Kawamura & Wasteneys, 2008; Ma et al, 2021). Microtubule‐associated proteins (MAPs) critically regulate the function and arrangement of MTs and are present in all known eukaryotic organisms with an overall high conservation.…”

“…The function of the nine Arabidopsis thaliana QWRF proteins remains mostly unclear; however, some of them have been found to be involved in dynamic modulation of cortical and mitotic MTs. For example, SCO3 ( At QWRF1) and At QWRF2 are involved in anisotropic cell expansion by interacting with cortical MTs, while AUG8 ( At QWRF8) and EDE1 ( At QWRF5) regulate the formation of spindle and phragmoplast MT arrays (Lee et al, 2017; Ma et al, 2021; Pignocchi et al, 2009). High evolutionary divergence within the AUG8/EDE1/QWRF family has rendered proteins with poor sequence homology (Lee et al, 2017).…”

“…AtQWRF1/ SCO3 AT3G19570 AtQWRF1/Snowy Cotyledon 3 (SCO3) participates in the development and anisotropic cell expansion of floral organs in connection with AtQWRF2. The qwrf1qwrf2 double mutant presents scattered microtubule (MT) bundles (Ma et al, 2021). The N-terminus of AtQWRF1 is basic and positively charged (similarly to other QWRF motif-containing proteins such as AUG8 and EDE1), indicating a putative role in MT-binding (Lee et al, 2017).…”

“…AtQWRF2 participates in development and anisotropic cell expansion of floral organs (in concert with AtQWRF1). AtQWRF2 lacks a PTS1 motif, but is functionally redundant to AtQWRF1 in floral organ growth (Ma et al, 2021) 659 aa, 44.92…”