A molecular mechanism for salt stress-induced microtubule array formation in Arabidopsis

Abstract

44Microtubules are filamentous structures necessary for cell division, motility and morphology, 45 with dynamics critically regulated by microtubule-associated proteins (MAPs). We outline 46 the molecular mechanism by which the MAP, COMPANION OF CELLULOSE 47 SYNTHASE1 (CC1), controls microtubule bundling and dynamics to sustain plant growth 48 under salt stress. CC1 contains an intrinsically disordered N-terminus that links microtubules 49 at evenly distributed distances through four conserved hydrophobic regions. NMR analyses 50 revealed that two neighboring residues in the first hydrophobic binding motif are crucial for 51 the microtubule interaction, which we confirmed through live cell analyses. The microtubule-52 binding mechanism of CC1 is remarkably similar to that of the prominent neuropathology-53 related protein Tau, indicating evolutionary convergence of MAP functions across animal and 54 plant cells. 55 56 Introduction 57 Microtubules are tubular structures essential to morphogenesis, division and motility in 58 eukaryotic cells 1 . While animal cells typically contain a centrosome with radiating 59 microtubules toward the cell periphery, growing plant cells arrange their microtubules along 60 the cell cortex 2 . A major function of the cortical microtubules in plant cells is to direct the 61 synthesis of cellulose, a fundamental component of the cell wall essential to plant 62 morphology 3 . Cellulose is produced at the plasma membrane by Cellulose Synthase (CESA) 63 protein complexes (CSCs; 4 ) that display catalytically-driven motility along the membrane 3 . 64 The recently described microtubule-associated protein (MAP), Companion of Cellulose 65 Synthase1 (CC1), is an integral component of the CSC and sustains cellulose synthesis by 66promoting the formation of a stress-tolerant microtubule array during salt stress 5 . As 67 cellulose synthesis is key for plant growth, engineering of plants to better produce cellulose is 68 of utmost importance to agriculture. Indeed, understanding the molecular mechanism by 69 which CC1 controls cellulose synthesis may bear opportunities to improve cultivation on salt-70 affected lands. 71The microtubule network is highly dynamic, and its state is influenced by the action 72 of MAPs. The mammalian Tau/MAP2/MAP4 family represents the most investigated MAP 73 set, primarily due to Tau's importance in the pathology of neurodegenerative diseases 6-8 . In 74 vitro, Tau promotes polymerization and bundling of microtubules, and diffuses along the 75 microtubule lattice 9-11 . In the brain, Tau is predominantly located at the axons of neurons, 76 where it contributes to the microtubule organization that drives neurite outgrowth 12,13 . In 77 disease, Tau self-aggregates into neurofibrillary tangles that might trigger neurodegeneration 78 14 . Intriguingly, no clear homologs of the Tau/MAP2/MAP4 family have been identified in 79 plants 15,16 . Because the full scope of Tau's biological role remains elusive, identification of 80 Tau-related proteins outside the anima...

Pathogen-induced pH changes regulate the growth-defense balance of plants

“…The CC proteins and more specifically the CC1 MT-binding domain are indispensable for the rearrangement of the CSC-MT machinery in response to salt stress (Endler et al , 2015;Kesten et al , 2018) . Consequently, mutants affected in CC function show stunted growth on salt containing media (Kesten et al , 2018) . Here, we show that the same CC1 domain is directly involved in the regulation of the CSC-MT machinery upon biotic stress.…”

“…This mutual support has been reported by several studies, especially under abiotic stress conditions such as drought and salt (Gutierrez et al , 2009;Nick, 2013;Endler et al , 2015;Wang et al , 2016) . Recently, CCs were shown to be indispensable for the recovery of the cortical MT array and CSC activity under salt stress (Endler et al , 2015) , and the microtubule interacting N-terminus of CC1 to be key for this function (Kesten et al , 2018) .…”

AtTRAPPC11 is involved in TRAPPIII mediated control of post-Golgi protein trafficking

“…4 We previously showed that AtTRAPPC11, and plausibly TRAPPIII, regulates SYP61-mediated post-Golgi trafficking. 4 Thus, it is tempting to speculate that defective trafficking of CESA6, BRI1, PIP1; and other PM residents critical the stress response, [19][20][21][22][23][24] evidenced by their abnormal intracellular accumulation, is responsible for the salt hypersensitivity of attrappc11.…”