LRX Proteins Play a Crucial Role in Pollen Grain and Pollen Tube Cell Wall Development

Fabrice, Tohnyui Ndinyanka; Vogler, Hannes; Draeger, Christian; Munglani, Gautam; Gupta, Shibu; Herger, Aline; Knox, John; Grossniklaus, Ueli; Ringli, Christoph

doi:10.1104/pp.17.01374

Cited by 82 publications

(58 citation statements)

References 55 publications

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“…We have previously shown that apoplastic LRX proteins associate with the plasma membrane and LRX4 binds to the transmembrane CrRLK1L FER [37,41]. This property of LRXs was investigated in more detail.…”

Section: The Membrane Association Of Lrx4 Is Independent Of Fermentioning

confidence: 99%

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Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis

et al. 2020

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Plant cell growth requires the coordinated expansion of the protoplast and the cell wall, which is controlled by an elaborate system of cell wall integrity (CWI) sensors linking the different cellular compartments. LRR-eXtensins (LRXs) are cell wall-attached extracellular regulators of cell wall formation and high-affinity binding sites for RALF (Rapid ALkalinization Factor) peptide hormones that trigger diverse physiological processes related to cell growth. LRXs function in CWI sensing and in the case of LRX4 of Arabidopsis thaliana, this activity was shown to involve interaction with the transmembrane Catharanthus roseus Receptor-Like Kinase1-Like (CrRLK1L) protein FERONIA (FER). Here, we demonstrate that binding of RALF1 and FER is common to most tested LRXs of vegetative tissue, including LRX1, the main LRX protein of root hairs. Consequently, an lrx1-lrx5 quintuple mutant line develops shoot and root phenotypes reminiscent of the fer-4 knockout mutant. The previously observed membrane-association of LRXs, however, is FER-independent, suggesting that LRXs bind not only FER but also other membrane-localized proteins to establish a physical link between intra-and extracellular compartments. Despite evolutionary diversification of various LRX proteins, overexpression of several chimeric LRX constructs causes cross-complementation of lrx mutants, indicative of comparable functions among members of this protein family. Suppressors of the pollen-growth defects induced by mutations in the CrRLK1Ls ANXUR1/2 also alleviate lrx1 lrx2-induced mutant root hair phenotypes. This suggests functional similarity of LRX-CrRLK1L signaling processes in very different cell types and indicates that LRX proteins are components of conserved processes regulating cell growth.

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Section: The Membrane Association Of Lrx4 Is Independent Of Fermentioning

confidence: 99%

“…Therefore, these results suggest that LRXs and FER function in a common process. The N-terminal moiety with the NT-and LRR-domains has been shown to associate with the membrane fraction [37], indicating a function of LRXs in linking the cell wall with the plasma membrane by binding of a membrane-localized interaction partner.…”

Section: Plos Geneticsmentioning

confidence: 99%

Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis

et al. 2020

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“…The polarized and rapid growth of the pollen tube cell depends on the highly dynamic remodeling of its cell wall. The redundant signaling peptides RALF4 and RALF19 ensure pollen tube integrity and growth by interacting with two distinct protein families, the malectin-domain CrRLK1L membrane receptor kinases (1)(2)(3) and the cell-wall monitoring leucine-rich repeat (LRR) extensin proteins (LRXs) (4,5).…”

Section: Introductionmentioning

confidence: 99%

Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth

Moussu

Broyart

Santos-Fernandez

et al. 2019

Preprint

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J.S) ‡ These authors contributed equally to this work SignificancePlant reproduction relies on proper pollen tube growth to reach the female tissue and release the sperm cells. This process is highly regulated by a family of secreted signaling peptides that are recognized by cell-wall monitoring proteins to enable plant fertilization. Here, we report the crystal structure of the LRX-RALF cell-wall complex and we demonstrate that RALF peptides are active as folded proteins. RALFs are autocrine signaling proteins able to instruct LRX cell-wall modules and CrRKL1L receptors, through structurally different binding modes to coordinate pollen tube integrity. AbstractPlant reproduction relies on the highly regulated growth of the pollen tube for proper sperm delivery. This process is controlled by secreted RALF signaling peptides, which have been previously shown to be perceived by CrRLK1Ls membrane receptor-kinases and leucine-rich (LRR) extensin proteins (LRXs). Here we demonstrate that RALF peptides are active as folded, disulfide bond-stabilized proteins, which can bind to the LRR domain of LRX proteins with nanomolar affinity. Crystal structures of the LRX-RALF signaling complexes reveal LRX proteins as constitutive dimers. The N-terminal LRR domain containing the RALF binding site is tightly linked to the extensin domain via a cysteine-rich tail. Our biochemical and structural work reveals a complex signaling network by which RALF ligands may instruct different signaling proteins -here CrRLK1Ls and LRXs -through structurally different binding modes to orchestrate cell wall remodeling in rapidly growing pollen tubes.

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“…Tohnyui Ndinyanka Fabrice et al and Xiaoxiao Wang et al have recently reported similar findings on LRX8-11 [43,44]. It also has been shown that LRX8-11 interact with Arabidopsis pollen RALF peptides [45].…”

Section: Author Contributionsmentioning

confidence: 56%

Arabidopsis pollen extensins LRX are required for cell wall integrity during pollen tube growth

et al. 2018

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Proper cell wall assembly is crucial during pollen tube growth. Leucine-rich repeat extensins (LRXs) are extracellular glycoproteins which belong to the hydroxyproline-rich glycoprotein (HRGP) family. They contain a conserved N-terminal leucine-rich repeat (LRR) domain and a highly variable C-terminal extensin domain. Here, we characterized four LRX proteins (LRX8 through LRX11) from pollen of Arabidopsis thaliana. To investigate the role of LRX8-LRX11 in pollen germination and pollen tube growth, multiple T-DNA lrx mutants were obtained. The lrx mutants display abnormal pollen tubes with an irregular deposition of callose and pectin. They also show serious alterations in pollen germination and segregation ratio. Our results suggest that LRXs are involved in ensuring proper cell wall assembly during pollen tube growth.

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LRX Proteins Play a Crucial Role in Pollen Grain and Pollen Tube Cell Wall Development

Abstract: 29Leucine-rich repeat extensins (LRXs)

Cited by 82 publications

References 55 publications

Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis

Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis

Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth

Arabidopsis pollen extensins LRX are required for cell wall integrity during pollen tube growth

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