Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host
Many important fungal pathogens of plants spend long periods (days to weeks) of their infection cycle in symptomless association with living host tissue, followed by a sudden transition to necrotrophic feeding as host tissue death occurs. Little is known about either the host responses associated wi...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
The American Phytopathological Society
2007-02-01
|
| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-20-2-0178 |
| _version_ | 1811291397446172672 |
|---|---|
| author | John Keon John Antoniw Raffaella Carzaniga Siân Deller Jane L. Ward John M. Baker Michael H. Beale Kim Hammond-Kosack Jason J. Rudd |
| author_facet | John Keon John Antoniw Raffaella Carzaniga Siân Deller Jane L. Ward John M. Baker Michael H. Beale Kim Hammond-Kosack Jason J. Rudd |
| author_sort | John Keon |
| collection | DOAJ |
| description | Many important fungal pathogens of plants spend long periods (days to weeks) of their infection cycle in symptomless association with living host tissue, followed by a sudden transition to necrotrophic feeding as host tissue death occurs. Little is known about either the host responses associated with this sudden transition or the specific adaptations made by the pathogen to invoke or tolerate it. We are studying a major host-specific fungal pathogen of cultivated wheat, Septoria tritici (teleomorph Mycosphaerella graminicola). Here, we describe the host responses of wheat leaves infected with M. graminicola during the development of disease symptoms and use microarray transcription profiling to identify adaptive responses of the fungus to its changing environment. We show that symptom development on a susceptible host genotype has features reminiscent of the hypersensitive response, a rapid and strictly localized form of host programmed cell death (PCD) more commonly associated with disease-resistance mechanisms. The initiation and advancement of this host response is associated with a loss of cell-membrane integrity and dramatic increases in apoplastic metabolites and the rate of fungal growth. Micro-array analysis of the fungal genes differentially expressed before and after the onset of host PCD supports a transition to more rapid growth. Specific physiological adaptation of the fungus is also revealed with respect to membrane transport, chemical and oxidative stress mechanisms, and metabolism. Our data support the hypothesis that host plant PCD plays an important role in susceptibility towards fungal pathogens with necrotrophic lifestyles. |
| first_indexed | 2024-04-13T04:28:47Z |
| format | Article |
| id | doaj.art-9ef52a8358ac45fda8742df19d3c51d1 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-04-13T04:28:47Z |
| publishDate | 2007-02-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-9ef52a8358ac45fda8742df19d3c51d12022-12-22T03:02:24ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062007-02-0120217819310.1094/MPMI-20-2-0178Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat HostJohn KeonJohn AntoniwRaffaella CarzanigaSiân DellerJane L. WardJohn M. BakerMichael H. BealeKim Hammond-KosackJason J. RuddMany important fungal pathogens of plants spend long periods (days to weeks) of their infection cycle in symptomless association with living host tissue, followed by a sudden transition to necrotrophic feeding as host tissue death occurs. Little is known about either the host responses associated with this sudden transition or the specific adaptations made by the pathogen to invoke or tolerate it. We are studying a major host-specific fungal pathogen of cultivated wheat, Septoria tritici (teleomorph Mycosphaerella graminicola). Here, we describe the host responses of wheat leaves infected with M. graminicola during the development of disease symptoms and use microarray transcription profiling to identify adaptive responses of the fungus to its changing environment. We show that symptom development on a susceptible host genotype has features reminiscent of the hypersensitive response, a rapid and strictly localized form of host programmed cell death (PCD) more commonly associated with disease-resistance mechanisms. The initiation and advancement of this host response is associated with a loss of cell-membrane integrity and dramatic increases in apoplastic metabolites and the rate of fungal growth. Micro-array analysis of the fungal genes differentially expressed before and after the onset of host PCD supports a transition to more rapid growth. Specific physiological adaptation of the fungus is also revealed with respect to membrane transport, chemical and oxidative stress mechanisms, and metabolism. Our data support the hypothesis that host plant PCD plays an important role in susceptibility towards fungal pathogens with necrotrophic lifestyles.https://apsjournals.apsnet.org/doi/10.1094/MPMI-20-2-0178cytochrome c releaseDNA fragmentation1H-NMRMycosphaerella fijiensispycnidiareactive oxygen species |
| spellingShingle | John Keon John Antoniw Raffaella Carzaniga Siân Deller Jane L. Ward John M. Baker Michael H. Beale Kim Hammond-Kosack Jason J. Rudd Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host Molecular Plant-Microbe Interactions cytochrome c release DNA fragmentation 1H-NMR Mycosphaerella fijiensis pycnidia reactive oxygen species |
| title | Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host |
| title_full | Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host |
| title_fullStr | Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host |
| title_full_unstemmed | Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host |
| title_short | Transcriptional Adaptation of Mycosphaerella graminicola to Programmed Cell Death (PCD) of Its Susceptible Wheat Host |
| title_sort | transcriptional adaptation of mycosphaerella graminicola to programmed cell death pcd of its susceptible wheat host |
| topic | cytochrome c release DNA fragmentation 1H-NMR Mycosphaerella fijiensis pycnidia reactive oxygen species |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-20-2-0178 |
| work_keys_str_mv | AT johnkeon transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT johnantoniw transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT raffaellacarzaniga transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT siandeller transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT janelward transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT johnmbaker transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT michaelhbeale transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT kimhammondkosack transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost AT jasonjrudd transcriptionaladaptationofmycosphaerellagraminicolatoprogrammedcelldeathpcdofitssusceptiblewheathost |