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Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions.

Samuel M, Bleackley M, Anderson M, Mathivanan S - Front Plant Sci (2015)

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University Melbourne, VIC, Australia.

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Whilst the role of EVs in plant-fungal interactions is still poorly defined, this non-canonical secretory pathway has been proposed as an alternative route for the secretion of virulence and defense molecules by fungi and plants, respectively (Robatzek, ; Rodrigues et al., )... The basic requirement for successful host colonization is the establishment of a parasitic relationship between the fungal pathogen and the host... Furthermore, the isolated EVs were biologically active as they could invigorate phagocytes in the host and enhance their antimicrobial activity (Oliveira et al., )... Other mammalian fungal pathogens including Histoplasma capsulatum, Candida parapsilosis, Sporothrix schenckii, and Candida albicans also deliver a variety of effector molecules in a similar manner (Albuquerque et al., ; Vargas et al., ; Gil-Bona et al., )... Interestingly, the serum from patients with H. capsulatum infections contains antibodies to proteins that are present in the EVs produced by the pathogen indicating involvement of EVs in the host-pathogen interaction... Biochemical analyses of EVs from various human fungal pathogens has revealed the presence of a variety of lipids, proteins and RNA (Peres Da Silva et al., )... Recent findings pertaining to the role of EVs in the interaction between fungal pathogens and humans have led us to ask whether EVs also have a major role in plant pathogen interactions... It is still unknown how effectors and defense molecules are packaged and transported across the plasma membranes and cell walls of the plant and fungal cells... We propose that proteins lacking secretion signals could be packaged into EVs for passage through the plasma membrane and the cell wall (Figure 1)... Alternatively, proteins containing a secretion signal could be secreted into the matrix of the cell wall and then bind to EVs via a lipid binding motif... Based on the discovery that EVs aid disease progression (Boukouris and Mathivanan, ; Gangoda et al., ), we propose that EVs can mediate/aid in fungal infection... This could be achieved via the transfer of effectors via EVs and/or by modulating the host cells response in favor of the fungal pathogen... Investigation of the role of EVs in plant-fungal interactions is likely to uncover a new mechanism for delivery and identification of molecules required for a productive infection and/or defense response... This knowledge will enhance our ability to protect agricultural crops against the damaging effects of fungal pathogens and securing our food sources for generations to come.

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Schematic representation of putative crosstalk via EVs at the plant-fungal interface. Exosome biogenesis and secretion in the fungal side: MVBs are formed from the early endosomes. Within the MVBs, invagination of the limiting membrane results in the formation of intraluminal vesicles which are packaged with protein and RNA cargo from the cell. The MVBs either fuse with the plasma membrane or with the lysosome for degradation. When the MVBs fuse with the plasma membrane, the intraluminal vesicles are released as exosomes. The exosomes are considered to contain various molecules including effectors that are required for the establishment of the pathogen and/or infection. Exosome biogenesis and secretion in the plant side: Similarly, on the plant side, vesicles from the MVBs may contain innate immunity proteins and defense molecules that can impede fungal growth or lead to alterations in the fungal cell wall. Thus, the plant and its fungal counterpart could utilize the exosomes as one of the many strategies in their mutual struggle for survival.
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Figure 1: Schematic representation of putative crosstalk via EVs at the plant-fungal interface. Exosome biogenesis and secretion in the fungal side: MVBs are formed from the early endosomes. Within the MVBs, invagination of the limiting membrane results in the formation of intraluminal vesicles which are packaged with protein and RNA cargo from the cell. The MVBs either fuse with the plasma membrane or with the lysosome for degradation. When the MVBs fuse with the plasma membrane, the intraluminal vesicles are released as exosomes. The exosomes are considered to contain various molecules including effectors that are required for the establishment of the pathogen and/or infection. Exosome biogenesis and secretion in the plant side: Similarly, on the plant side, vesicles from the MVBs may contain innate immunity proteins and defense molecules that can impede fungal growth or lead to alterations in the fungal cell wall. Thus, the plant and its fungal counterpart could utilize the exosomes as one of the many strategies in their mutual struggle for survival.

Mentions: Recent findings pertaining to the role of EVs in the interaction between fungal pathogens and humans have led us to ask whether EVs also have a major role in plant pathogen interactions. It is still unknown how effectors and defense molecules are packaged and transported across the plasma membranes and cell walls of the plant and fungal cells. We propose that proteins lacking secretion signals could be packaged into EVs for passage through the plasma membrane and the cell wall (Figure 1). Alternatively, proteins containing a secretion signal could be secreted into the matrix of the cell wall and then bind to EVs via a lipid binding motif. The protein then transits the cell wall as a passenger on the outer leaflet of the vesicle. Based on the discovery that EVs aid disease progression (Boukouris and Mathivanan, 2015; Gangoda et al., 2015), we propose that EVs can mediate/aid in fungal infection. This could be achieved via the transfer of effectors via EVs and/or by modulating the host cells response in favor of the fungal pathogen. Similarly, we propose that plant EVs can aid in the protection against pathogenic infections. Upon infection, defense molecules can be packaged and delivered to the site of infection to protect against the invading pathogen. Further to this, we propose that the molecular cargo present in EVs is specific to the type of insult or infection. For instance, molecular cargo present in EVs of plants during stress can be significantly different to that produced during fungal infection. Thus the molecular cargo contained within EVs of plant or fungus can serve as indicators of health, stress, and disease. Investigation of the role of EVs in plant-fungal interactions is likely to uncover a new mechanism for delivery and identification of molecules required for a productive infection and/or defense response. This knowledge will enhance our ability to protect agricultural crops against the damaging effects of fungal pathogens and securing our food sources for generations to come.


Extracellular vesicles including exosomes in cross kingdom regulation: a viewpoint from plant-fungal interactions.

Samuel M, Bleackley M, Anderson M, Mathivanan S - Front Plant Sci (2015)

Schematic representation of putative crosstalk via EVs at the plant-fungal interface. Exosome biogenesis and secretion in the fungal side: MVBs are formed from the early endosomes. Within the MVBs, invagination of the limiting membrane results in the formation of intraluminal vesicles which are packaged with protein and RNA cargo from the cell. The MVBs either fuse with the plasma membrane or with the lysosome for degradation. When the MVBs fuse with the plasma membrane, the intraluminal vesicles are released as exosomes. The exosomes are considered to contain various molecules including effectors that are required for the establishment of the pathogen and/or infection. Exosome biogenesis and secretion in the plant side: Similarly, on the plant side, vesicles from the MVBs may contain innate immunity proteins and defense molecules that can impede fungal growth or lead to alterations in the fungal cell wall. Thus, the plant and its fungal counterpart could utilize the exosomes as one of the many strategies in their mutual struggle for survival.
© Copyright Policy
Related In: Results  -  Collection

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Figure 1: Schematic representation of putative crosstalk via EVs at the plant-fungal interface. Exosome biogenesis and secretion in the fungal side: MVBs are formed from the early endosomes. Within the MVBs, invagination of the limiting membrane results in the formation of intraluminal vesicles which are packaged with protein and RNA cargo from the cell. The MVBs either fuse with the plasma membrane or with the lysosome for degradation. When the MVBs fuse with the plasma membrane, the intraluminal vesicles are released as exosomes. The exosomes are considered to contain various molecules including effectors that are required for the establishment of the pathogen and/or infection. Exosome biogenesis and secretion in the plant side: Similarly, on the plant side, vesicles from the MVBs may contain innate immunity proteins and defense molecules that can impede fungal growth or lead to alterations in the fungal cell wall. Thus, the plant and its fungal counterpart could utilize the exosomes as one of the many strategies in their mutual struggle for survival.
Mentions: Recent findings pertaining to the role of EVs in the interaction between fungal pathogens and humans have led us to ask whether EVs also have a major role in plant pathogen interactions. It is still unknown how effectors and defense molecules are packaged and transported across the plasma membranes and cell walls of the plant and fungal cells. We propose that proteins lacking secretion signals could be packaged into EVs for passage through the plasma membrane and the cell wall (Figure 1). Alternatively, proteins containing a secretion signal could be secreted into the matrix of the cell wall and then bind to EVs via a lipid binding motif. The protein then transits the cell wall as a passenger on the outer leaflet of the vesicle. Based on the discovery that EVs aid disease progression (Boukouris and Mathivanan, 2015; Gangoda et al., 2015), we propose that EVs can mediate/aid in fungal infection. This could be achieved via the transfer of effectors via EVs and/or by modulating the host cells response in favor of the fungal pathogen. Similarly, we propose that plant EVs can aid in the protection against pathogenic infections. Upon infection, defense molecules can be packaged and delivered to the site of infection to protect against the invading pathogen. Further to this, we propose that the molecular cargo present in EVs is specific to the type of insult or infection. For instance, molecular cargo present in EVs of plants during stress can be significantly different to that produced during fungal infection. Thus the molecular cargo contained within EVs of plant or fungus can serve as indicators of health, stress, and disease. Investigation of the role of EVs in plant-fungal interactions is likely to uncover a new mechanism for delivery and identification of molecules required for a productive infection and/or defense response. This knowledge will enhance our ability to protect agricultural crops against the damaging effects of fungal pathogens and securing our food sources for generations to come.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Microbiology, School of Life Sciences, La Trobe University Melbourne, VIC, Australia.

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

Whilst the role of EVs in plant-fungal interactions is still poorly defined, this non-canonical secretory pathway has been proposed as an alternative route for the secretion of virulence and defense molecules by fungi and plants, respectively (Robatzek, ; Rodrigues et al., )... The basic requirement for successful host colonization is the establishment of a parasitic relationship between the fungal pathogen and the host... Furthermore, the isolated EVs were biologically active as they could invigorate phagocytes in the host and enhance their antimicrobial activity (Oliveira et al., )... Other mammalian fungal pathogens including Histoplasma capsulatum, Candida parapsilosis, Sporothrix schenckii, and Candida albicans also deliver a variety of effector molecules in a similar manner (Albuquerque et al., ; Vargas et al., ; Gil-Bona et al., )... Interestingly, the serum from patients with H. capsulatum infections contains antibodies to proteins that are present in the EVs produced by the pathogen indicating involvement of EVs in the host-pathogen interaction... Biochemical analyses of EVs from various human fungal pathogens has revealed the presence of a variety of lipids, proteins and RNA (Peres Da Silva et al., )... Recent findings pertaining to the role of EVs in the interaction between fungal pathogens and humans have led us to ask whether EVs also have a major role in plant pathogen interactions... It is still unknown how effectors and defense molecules are packaged and transported across the plasma membranes and cell walls of the plant and fungal cells... We propose that proteins lacking secretion signals could be packaged into EVs for passage through the plasma membrane and the cell wall (Figure 1)... Alternatively, proteins containing a secretion signal could be secreted into the matrix of the cell wall and then bind to EVs via a lipid binding motif... Based on the discovery that EVs aid disease progression (Boukouris and Mathivanan, ; Gangoda et al., ), we propose that EVs can mediate/aid in fungal infection... This could be achieved via the transfer of effectors via EVs and/or by modulating the host cells response in favor of the fungal pathogen... Investigation of the role of EVs in plant-fungal interactions is likely to uncover a new mechanism for delivery and identification of molecules required for a productive infection and/or defense response... This knowledge will enhance our ability to protect agricultural crops against the damaging effects of fungal pathogens and securing our food sources for generations to come.

No MeSH data available.


Related in: MedlinePlus