Emerging roles of tetraspanins in plant inter-cellular and inter-kingdom communication

Abstract

Inter-cellular and inter-kingdom signaling systems of various levels of complexity regulate pathogenic and mutualistic interactions between bacteria, parasites, and fungi and animal and plant hosts. Interkingdom interactions between mutualistic bacteria such as rhizobia and legumes during nodulation and between fungi and plants during mycorrhizal associations, are characterized by the extensive exchange of molecular signals, which allow nitrogen and phosphate assimilation, respectively. A novel aspect of this signaling exchange is the existence of specific structures, the exosomes, that carry important molecules that shape the plant-pathogen interactions. Exosomes contain a wide array of molecules, such as lipids, proteins, messenger RNA, and microRNAs, that play important roles in cell-to-cell communication in animal and plant cells by affecting gene expression and other physiological activity in distant cells within the same organism (e.g., during cancer metastases and neuron injuries). In plant cells, it has been recently reported that exosomes go beyond organism boundaries and inhibit a pathogenic interaction in plants. Plant produce and send exosomes loaded with specific small miRNA which inhibit the pathogen infection, but the pathogen can also produce exosomes carrying propathogenic proteins and microRNAs. Therefore, exosomes are the important bridge regulating the signal exchange. Exosomes are small membrane-bound vesicles derived from multivesicular bodies (MVBs), which carries selected cargos from the cytoplasm (protein, lipids, and microRNAs) and under certain circumstances, they fuse with the plasma membrane, releasing the small vesicles as cargo-carrying exosomes into the extracellular space during intercellular and inter-kingdom communication. Animal and plant proteomic studies have demonstrated that tetraspanin proteins are an integral part of exosome membranes, positioning tetraspanins as essential components for endosome organization, with key roles in membrane fusion, cell trafficking, and membrane recognition. We discuss the similarities and differences between animal tetraspanins and plant tetraspanins formed during plant-microbe interactions and their potential role in mutualistic communication.

Membrane Transporters in Citrus clementina Fruit Juice-Derived Nanovesicles

“…Tetraspanins CD9, CD63, and CD81 are frequently present in EV samples and are often used as EV biomarkers. Plant tetraspanins have been overlooked for a long time but research is emerging thanks to their newly discovered roles in intercellular and interspecies communication [22]. Seventeen tetraspanin genes have been described in the model plant Arabidopsis.…”

De novo Assembly of Transcriptomes From a B73 Maize Line Introgressed With a QTL for Resistance to Gray Leaf Spot Disease Reveals a Candidate Allele of a Lectin Receptor-Like Kinase

“…In this study, a calcineurin-B-like protein, two calmodulins, and a calciumdependent lipid-binding protein were expressed in B73-QTL in response to the pathogen. Vesicular trafficking is regarded as an important part of plant defense so that anti-microbial cargoes can be delivered to sites of infection, including small RNAs; therefore, it is significant that a tetraspanin and an exocyst component SEC6 were identified (Jimenez-Jimenez et al, 2019).…”

In situ and ex situ imaging of plant extracellular vesicles as nanovectors for cross‐domain communication

“…Tetraspanins are proteins with four membrane‐spanning domains, with 17 members identified in A . thaliana (Jimenez‐Jimenez et al., 2019). These results support the cross‐kingdom RNA interference (RNAi) by plant exosomes (Rutter & Innes, 2018).…”

“…Ap, appressorium; Hy, hypha; MVB, multivesicular body; PAM, periarbuscular membrane; PAS, periarbuscular space. From Jimenez‐Jimenez et al., 2019 with permission from the publisher [Colour figure can be viewed at wileyonlinelibrary.com]…”