Cargando…

Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking

Cytokinin (CK) is an important plant developmental regulator, having activities in many aspects of plant life and response to the environment. CKs are involved in diverse processes in the plant, including stem cell maintenance, vascular differentiation, growth and branching of roots and shoots, leaf...

Descripción completa

Detalles Bibliográficos
Autores principales: Gupta, Rupali, Anand, Gautam, Pizarro, Lorena, Laor Bar-Yosef, Dana, Kovetz, Neta, Sela, Noa, Yehuda, Tal, Gazit, Ehud, Bar, Maya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524340/
https://www.ncbi.nlm.nih.gov/pubmed/34663100
http://dx.doi.org/10.1128/mBio.03068-20
_version_ 1784585495173398528
author Gupta, Rupali
Anand, Gautam
Pizarro, Lorena
Laor Bar-Yosef, Dana
Kovetz, Neta
Sela, Noa
Yehuda, Tal
Gazit, Ehud
Bar, Maya
author_facet Gupta, Rupali
Anand, Gautam
Pizarro, Lorena
Laor Bar-Yosef, Dana
Kovetz, Neta
Sela, Noa
Yehuda, Tal
Gazit, Ehud
Bar, Maya
author_sort Gupta, Rupali
collection PubMed
description Cytokinin (CK) is an important plant developmental regulator, having activities in many aspects of plant life and response to the environment. CKs are involved in diverse processes in the plant, including stem cell maintenance, vascular differentiation, growth and branching of roots and shoots, leaf senescence, nutrient balance, and stress tolerance. In some cases, phytopathogens secrete CKs. It has been suggested that to achieve pathogenesis in the host, CK-secreting biotrophs manipulate CK signaling to regulate the host cell cycle and nutrient allocation. CK is known to induce host plant resistance to several classes of phytopathogens from a few works, with induced host immunity via salicylic acid signaling suggested to be the prevalent mechanism for this host resistance. Here, we show that CK directly inhibits the growth, development, and virulence of fungal phytopathogens. Focusing on Botrytis cinerea (Bc), we demonstrate that various aspects of fungal development can be reversibly inhibited by CK. We also found that CK affects both budding and fission yeast in a similar manner. Investigating the mechanism by which CK influences fungal development, we conducted RNA next-generation sequencing (RNA-NGS) on mock- and CK-treated B. cinerea samples, finding that CK alters the cell cycle, cytoskeleton, and endocytosis. Cell biology experiments demonstrated that CK affects cytoskeleton components and cellular trafficking in Bc, lowering endocytic rates and endomembrane compartment sizes, likely leading to reduced growth rates and arrested developmental programs. Mutant analyses in yeast confirmed that the endocytic pathway is altered by CK. Our work uncovers a remarkably conserved role for a plant growth hormone in fungal biology, suggesting that pathogen-host interactions resulted in fascinating molecular adaptations on fundamental processes in eukaryotic biology.
format Online
Article
Text
id pubmed-8524340
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-85243402021-10-20 Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking Gupta, Rupali Anand, Gautam Pizarro, Lorena Laor Bar-Yosef, Dana Kovetz, Neta Sela, Noa Yehuda, Tal Gazit, Ehud Bar, Maya mBio Research Article Cytokinin (CK) is an important plant developmental regulator, having activities in many aspects of plant life and response to the environment. CKs are involved in diverse processes in the plant, including stem cell maintenance, vascular differentiation, growth and branching of roots and shoots, leaf senescence, nutrient balance, and stress tolerance. In some cases, phytopathogens secrete CKs. It has been suggested that to achieve pathogenesis in the host, CK-secreting biotrophs manipulate CK signaling to regulate the host cell cycle and nutrient allocation. CK is known to induce host plant resistance to several classes of phytopathogens from a few works, with induced host immunity via salicylic acid signaling suggested to be the prevalent mechanism for this host resistance. Here, we show that CK directly inhibits the growth, development, and virulence of fungal phytopathogens. Focusing on Botrytis cinerea (Bc), we demonstrate that various aspects of fungal development can be reversibly inhibited by CK. We also found that CK affects both budding and fission yeast in a similar manner. Investigating the mechanism by which CK influences fungal development, we conducted RNA next-generation sequencing (RNA-NGS) on mock- and CK-treated B. cinerea samples, finding that CK alters the cell cycle, cytoskeleton, and endocytosis. Cell biology experiments demonstrated that CK affects cytoskeleton components and cellular trafficking in Bc, lowering endocytic rates and endomembrane compartment sizes, likely leading to reduced growth rates and arrested developmental programs. Mutant analyses in yeast confirmed that the endocytic pathway is altered by CK. Our work uncovers a remarkably conserved role for a plant growth hormone in fungal biology, suggesting that pathogen-host interactions resulted in fascinating molecular adaptations on fundamental processes in eukaryotic biology. American Society for Microbiology 2021-10-19 /pmc/articles/PMC8524340/ /pubmed/34663100 http://dx.doi.org/10.1128/mBio.03068-20 Text en Copyright © 2021 Gupta et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Gupta, Rupali
Anand, Gautam
Pizarro, Lorena
Laor Bar-Yosef, Dana
Kovetz, Neta
Sela, Noa
Yehuda, Tal
Gazit, Ehud
Bar, Maya
Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title_full Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title_fullStr Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title_full_unstemmed Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title_short Cytokinin Inhibits Fungal Development and Virulence by Targeting the Cytoskeleton and Cellular Trafficking
title_sort cytokinin inhibits fungal development and virulence by targeting the cytoskeleton and cellular trafficking
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524340/
https://www.ncbi.nlm.nih.gov/pubmed/34663100
http://dx.doi.org/10.1128/mBio.03068-20
work_keys_str_mv AT guptarupali cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT anandgautam cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT pizarrolorena cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT laorbaryosefdana cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT kovetzneta cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT selanoa cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT yehudatal cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT gazitehud cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking
AT barmaya cytokinininhibitsfungaldevelopmentandvirulencebytargetingthecytoskeletonandcellulartrafficking