Cell wall integrity (CWI) maintenance is central for plant cells. Mechanical and chemical distortions, pH changes, and breakdown products of cell wall polysaccharides activate plasma membrane-localized receptors and induce appropriate downstream responses. Microbial interactions alter or destroy the structure of the plant cell wall, connecting CWI maintenance to immune responses. Cellulose is the major polysaccharide in the primary and secondary cell wall. Its breakdown generates short-chain cellooligomers that induce Ca2+-dependent CWI responses. We show that these responses require the malectin domain-containing CELLOOLIGOMER-RECEPTOR KINASE 1 (CORK1) in Arabidopsis and are preferentially activated by cellotriose (CT). CORK1 is required for cellooligomer-induced cytoplasmic Ca2+ elevation, reactive oxygen species (ROS) production, mitogen-associated protein kinase (MAPK) activation, cellulose synthase phosphorylation, and the regulation of CWI-related genes, including those involved in biosynthesis of cell wall material, secondary metabolites and tryptophan. Phosphoproteome analyses identified early targets involved in signaling, cellulose synthesis, the endoplasmic reticulum/Golgi secretory pathway, cell wall repair and immune responses. Two conserved phenylalanine residues in the malectin domain are crucial for CORK1 function. We propose that CORK1 is required for CWI and immune responses activated by cellulose breakdown products.
Plants host numerous endophytic microbes which promote plant performance, in particular under stress. A new endophytic fungus was isolated from the leaves of a deciduous wood tree Leucas aspera. Morphological inspection and multilocus phylogeny identified the fungus as a new Trichoderma strain. If applied to Arabidopsis thaliana and Nicotiana attenuata, it mainly colonizes their roots and strongly promotes initial growth of the plants on soil. The fungus grows on high NaCl or mannitol concentrations, and shows predatory capability on the pathogenic fungus Alternaria brassicicola. Colonized Arabidopsis plants tolerate higher salt stress and show lower A. brassicicola spread in roots and shoots, while arbuscular mycorrhiza formation in N. attenuata is not affected by the Trichoderma strain. These beneficial features of the novel Trichoderma strain are important prerequisites for agricultural applications.
Phosphate (Pi) availability has a strong influence on the symbiotic interaction between Arabidopsis and a recently described root-colonizing beneficial Trichoderma harzianum strain. When transferred to media with insoluble Ca3(PO4)2 as a sole Pi source, Arabidopsis seedlings died after 10 days. Trichoderma grew on the medium containing Ca3(PO4)2 and the fungus did colonize in roots, stems, and shoots of the host. The efficiency of the photosynthetic electron transport of the colonized seedlings grown on Ca3(PO4)2 medium was reduced and the seedlings died earlier, indicating that the fungus exerts an additional stress to the plant. Interestingly, the fungus initially alleviated the Pi starvation response and did not activate defense responses against the hyphal propagation. However, in colonized roots, the sucrose transporter genes SWEET11 and -12 were strongly down-regulated, restricting the unloading of sucrose from the phloem parenchyma cells to the apoplast. Simultaneously, up-regulation of SUC1 promoted sucrose uptake from the apoplast into the parenchyma cells and of SWEET2 sequestration of sucrose in the vacuole of the root cells. We propose that the fungus tries to escape from the Ca3(PO4)2 medium and colonizes the entire host. To prevent excessive sugar consumption by the propagating hyphae, the host restricts sugar availability in its apoplastic root space by downregulating sugar transporter genes for phloem unloading, and by upregulating transporter genes which maintain the sugar in the root cells.
The integrity of the cell wall is important for plant cells. Mechanical or chemical distortions, tension, pH changes in the apoplast, disturbance of the ion homeostasis, leakage of cell compounds into the apoplastic space or breakdown of cell wall polysaccharides activate cellular responses which often occur via plasma membrane-localized receptors. Breakdown products of the cell wall polysaccharides function as damage-associated molecular patterns and derive from cellulose (cello-oligomers), hemicelluloses (mainly xyloglucans and mixed-linkage glucans as well as glucuronoarabinoglucans in Poaceae) and pectins (oligogalacturonides). In addition, several types of channels participate in mechanosensing and convert physical into chemical signals. To establish a proper response, the cell has to integrate information about apoplastic alterations and disturbance of its wall with cell-internal programs which require modifications in the wall architecture due to growth, differentiation or cell division. We summarize recent progress in pattern recognition receptors for plant-derived oligosaccharides, with a focus on malectin domain-containing receptor kinases and their crosstalk with other perception systems and intracellular signaling events.
We have recently demonstrated that the cellulose breakdown product cellotriose is a damage-associated molecular pattern (DAMP) which induces responses related to the integrity of the cell wall. Activation of downstream responses requires the Arabidopsis malectin domain-containing CELLOOLIGOMER RECEPTOR KINASE1 (CORK1) 1 . The cellotriose/CORK1 pathway induces immune responses, including NADPH oxidase-mediated reactive oxygen species production, mitogen-activated protein kinase 3/6 phosphorylation-dependent defense gene activation, and the biosynthesis of defense hormones. However, apoplastic accumulation of cell wall breakdown products should also activate cell wall repair mechanisms. We demonstrate that the phosphorylation pattern of numerous proteins involved in the accumulation of an active cellulose synthase complex in the plasma membrane and those for protein trafficking to and within the trans -Golgi network (TGN) are altered within minutes after cellotriose application to Arabidopsis roots. The phosphorylation pattern of enzymes involved in hemicellulose or pectin biosynthesis and the transcript levels for polysaccharide-synthesizing enzymes responded barely to cellotriose treatments. Our data show that the phosphorylation pattern of proteins involved in cellulose biosynthesis and trans -Golgi trafficking is an early target of the cellotriose/CORK1 pathway.
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